1 Update Review 1 2 Short title: 3 Flower Central Metabolism 4 5 Corresponding author: 6 Monica Borghi 7 ORCID ID: 0000-0003-1359-7611 8 Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany. 9 E-mail: [email protected]10 11 Title: 12 Floral Metabolism of Sugars and Amino Acids: Implications for Pollinators’ Preferences and 13 Seed and Fruit Set 14 15 Authors’ names: 16 Monica Borghi 17 Alisdair R. Fernie 18 19 Authors’ affiliation: 20 Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany. 21 22 Funding: 23 This work was supported by the Marie Skłodowska-Curie Actions Individual Fellowship program 24 (grant no. 656918 to M.B.). 25 26 Plant Physiology Preview. Published on October 6, 2017, as DOI:10.1104/pp.17.01164 Copyright 2017 by the American Society of Plant Biologists
56
Embed
Update Review Short title6 105 2010). Indeed, early studies conducted with symplasmic tracers revealed that the trafficking 106 toward the apical meristem decreases after floral induction
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
1
Update Review 1
2
Short title: 3
Flower Central Metabolism 4
5
Corresponding author: 6
Monica Borghi 7
ORCID ID: 0000-0003-1359-7611 8
Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany. 9
Floral bacteria received far less attention than yeasts, until pyrosequencing and culturing 460
techniques made it possible to identify the strains that grow on flowers (Fridman et al., 2012; 461
Junker and Keller, 2015). Similarly to yeast, bacterial growth also negatively correlates with total 462
sugar content and/or sucrose content in nectar, but usually positively correlates with the 463
proportion of the monosaccharide fructose (Vannette et al., 2013; Lenaerts et al., 2016; Vannette 464
and Fukami, 2016). In addition, bacterial isolates of the genus Acinetobacter can convert sucrose 465
into a mucous matrix of polysaccharides (Fridman et al., 2012) (Fig. 1F). 466
20
Although the chemical modifications of nectar by yeasts and bacteria look very similar, the 467
effects on pollinators' preferences frequently diverge. The presence of bacterial colonies on floral 468
nectar often has negative effects on pollination success (Vannette et al., 2013) and insect 469
visitation rate (Junker et al., 2014). Conversely, nectar inoculated with yeasts results in increased 470
seed set of bumblebee- and hummingbird-pollinated flowers (Vannette et al., 2013), as well as 471
enhanced pollen donation via increment of pollinator foraging rate (Schaeffer and Irwin, 2014). 472
Nectar modifications of the amino acids content represent a small and under investigated field of 473
research. However, early observations suggest that bacteria may cause a reduction of specific 474
amino acids such as threonine and valine (Lenaerts et al., 2016). 475
476
477
Primary metabolites and pollinators’ preferences: implications for seed and fruit set 478
Seeds and fruits develop following a successful process of plant reproduction, which ultimately 479
depends upon the proper development of the stamen and pistil coupled to successful pollination 480
and fertilization events. Since floral primary metabolism is deeply intertwined with flower 481
development, aberrant floral metabolism can form a prezygotic barrier that prevents mating and 482
fertilization. For example, mutations that impair the metabolic processes of pollen and eggs 483
maturation, or interfere with pollen germination, tube growth and guidance (both in the pollen 484
and in the transmitting tissue) impede pollination and fertilization. As detrimental as these 485
mutations seem to be, they are favorably exploited in agriculture for example in the generation of 486
male sterile plants for hybrid breeding (Goetz et al., 2001; Hirsche et al., 2009). Neither as 487
equally well exploited nor understood, it is the influence that primary metabolism of nectar and 488
pollen has on pollinators’ preferences. Animal-pollinated plants depend upon insects, birds, and 489
mammals as go-betweens for pollen transfer. Therefore, their flowers produce signals (color and 490
scent) to attract pollinators, and nectar and pollen rewards to preserve floral fidelity. However, as 491
animal pollinators display preferences for quality and quantity of the reward, their choice to 492
21
pollinate, or not pollinate a flower affects fertilization and ultimately may reduce seed and fruit 493
set (Hanley et al., 2008; Carruthers et al., 2017). Insect preferences for flower color and odor 494
have been largely investigated and a few studies describe the link between plant genotype and 495
animal behavioral response (Bradshaw Jr and Schemske, 2003; Hoballah et al., 2007; Klahre et 496
al., 2011; Owen and Bradshaw, 2011; Yuan et al., 2013; Amrad et al., 2016; Sheehan et al., 497
2016). Instead, traditional single gene studies to ascertain pollinators’ responses to changes in 498
floral primary metabolism have been delayed by the late discovery of the SWEET9 transporter as 499
a mediator of nectar secretion (Lin et al., 2014), and so far, no transporter has been identified that 500
controls the secretion of amino acids in floral nectar (Zhou et al., 2016). However, a body of 501
growing evidence shows that primary metabolites of pollen and nectar are shaping the interaction 502
between plants and their pollinators through pollination syndromes (Johnson et al., 2006; Weiner 503
et al., 2010). That pollinators’ choices can affect nectar chemical composition was evident since 504
the early studies of Beker (1977) who observed that nectars are richer in amino acids if they are 505
the only source of protein-building material of the pollinators that feed on those. A similar 506
conclusion has been reached in more recent studies which showed that pollinators’ preference had 507
the most important effect on amino acid content in nectar, while taxonomical plant groups had a 508
weakly significant effect (Petanidou et al., 2006). For example, phenylalanine- and GABA-509
enriched nectars are commonly represented in plants pollinated by long-tongued bees and flies 510
independently from their taxonomical group. As GABA functions as an inhibitory 511
neurotransmitter of insects’ nervous system, GABA-rich nectar may be preferred for its calming 512
effect by pollinators (Nepi et al., 2012). Volume of secreted nectar also varies in response to 513
pollinators’ preferences and this happens more rapidly that initially thought. In fact, nectarless 514
plants in bumblebee-pollinated plants appear in a time as short as ten generations (Gervasi and 515
Schiestl, 2017). Pollen chemistry may have a weaker influence on insect preferences as polylectic 516
bees, which collect pollen from plants of different species appear to disregard the chemical 517
composition of pollen despite the beneficial effect that blends of amino acids and polypeptide 518
22
have on colony fitness (Vanderplanck et al., 2014). However, this may not hold true for 519
oligolectic bees, for which pollen chemistry drive evolutionary host-shifts (Vanderplanck et al., 520
2017). These studies and many others present in the literature demonstrate that pollen and nectar 521
chemistry influence pollinators’ choices, but that the interaction is specific between a plant and its 522
pollinators. In addition, it should be considered that very little is known about the transcriptional 523
and post-transcriptional regulation of floral primary metabolism, and how metabolism changes in 524
response to environmental fluctuations (e.g. temperature and rainfall), which may, ultimately, 525
also affect pollination and fertilization success (Gallagher and Campbell, 2017). 526
527
Conclusions and Perspective 528
The current knowledge on flower central metabolism is largely inferred from experiments 529
performed in leaves and it is certainly skewed by the generally accepted prejudice that flowers are 530
entirely heterotrophic. However, we have seen that cycles of carbohydrate hydrolysis and re-531
synthesis are functional and activated in flowers, as well as they are the routes for the 532
biosynthesis of amino acids and peptides. Therefore, there are many unsolved issues concerning 533
floral central metabolism, and the implications for flower development, pollinators’ choices, and 534
seed and fruit set (see Outstanding Questions). The investigations on floral metabolism have 535
certainly been made difficult by the redundant number of transporters of sugars and amino acids 536
which on one side warrant pollination and fertilization success to the plant, but on the other add 537
complexity to a deep understanding of single gene function. In addition, studies performed on 538
knockout mutants focused on the leaf or root phenotypes, and only rarely on flower physiology. 539
Largely under investigated is the measure by which floral metabolism depends on de novo 540
biosynthesis versus intake of sugars and amino acids. There is also a lack of knowledge 541
concerning the spatial distribution of metabolites in floral tissues and their physiological and 542
ecological significance. In addition, analysis of metabolites is often conducted on individual 543
flowers (or inflorescences) that are regarded as integral floral units, despite the fact that in no 544
23
other plant organ as much as in flowers, tissue compartmentalization underlies function. In 545
addition, floral metabolism dramatically changes multiple times in response to development, and 546
presumably, to environmental cues (Lauxmann et al., 2016). Recent advances in analytical 547
techniques that couple metabolomics with histological imaging can now be employed to shed 548
light on this topic (Dong et al., 2016). Techniques of rapid sequencing coupled with genome wide 549
association studies (GWAS) and quantitative trait locus (QTL) analysis promise to speed the 550
discovery rate of genes and the network of genes that control plant-pollinator interactions (Clare 551
et al., 2013; Sedio, 2017). Moreover, with the use of the CRISPR/Cas9 technology the link 552
between a plant genotype, floral chemotype, and pollinator response will likely be possible in 553
non-model organisms. 554
In conclusion, floral biology has become an intense area of study for scientists with expertise in 555
the most disparate disciplines encompassing plant developmental biology, molecular biology, 556
metabolomics and genomics, entomology, and behavioral biology. As described above, recent 557
advances in particular in understanding sugar transport, pollen tube growth, and in better 558
characterizing the chemical composition of nectar provide a firm foundation to comprehend the 559
link between floral metabolism and function. That said, it is our belief that today, as never before 560
a more holistic and collaborative approach is demanded to shed light on the mechanisms that 561
control floral metabolism and the implications for flower development and plant-pollinator 562
interactions. 563
564
565
566
24
Table 1 567
568
Table 1. Overview of the sugar transporters expressed in flowers of Arabidopsis thaliana, organ and tissue of expression, transported substrate, and associated mutant phenotype
Figure 1. Sugar partitioning in floral tissues. A, Unload of sucrose from the terminal phloem: 572
SUGAR WILL EVENTUALLY BE TRANSPORTED TRANSPORTERS (SWEET) are likely 573
been involved in the process. Cell wall invertase (cwINV) enzymes in the apoplasmic space 574
hydrolyze sucrose to glucose and fructose. SUCROSE TRANSPORTERS (SUTs) alternatively 575
called SUCROSE CARRIERs (SUCs) and SUGAR TRANSPORTER PROTEINS (STPs) carry 576
sucrose and hexose across the plasma membrane of the receptacle cells where carbohydrates are 577
stored as transitory starch. B, In the receptacle, sucrose and hexoses are symplasmically 578
transferred to the anthers. C, cwINVs and sucrose synthases (SUS) hydrolyze sucrose to hexoses, 579
which are transported in the tapetum by SUC/SUT and STP transporters. In the tapetum while it 580
develops, carbohydrates are stored as transitory starch, which is later converted to sucrose by the 581
combined activity of sucrose phosphate synthases (SPS) and sucrose phosphate phosphatase 582
(SPP). D, Pollen grains are apoplasmically isolated and take up sucrose and hexoses via 583
SUC/SUT and STP proteins. In developing pollen grains glucose-6-phosphate is transported 584
across the membrane of amyloplasts by GLUCOSE PHOSPHATE TRANSPORTER 1. Later 585
during development, glucose released by the amyloplasts is internalized in the vacuole by the 586
activity of VACUOLAR GLUCOSE TRANSPORTER 1 (VGT1) and utilized for sucrose 587
synthesis. Depending upon the species, droplets of lipids may also accumulate in mature pollen 588
grains. E, Pollen tube elongation is fuelled by sugars secreted by the transmitting tissue. Hexoses 589
are released in the transmitting tissue by the combined activity of cwINV of pollen grain (♂) and 590
stigma (♀), and by stigma specific vacuolar invertases (VIN). F, SUC/SUT and STP in the cells 591
of the nectary parenchyma take up sucrose and hexoses that are stored as starch granules. Before 592
anthesis, transitory starch is converted to sucrose that is exported by SWEET proteins to the 593
apoplasmic space for nectar secretion. Here, cwINVs hydrolyze sucrose to fructose and glucose. 594
Alternatively, fermentation reactions carried out by colonizing yeasts and bacteria modify the 595
28
sugar composition of nectar by releasing hexoses. Sometimes, the production of a mucous matrix 596
of polysaccharides has also been observed. 597
598
Figure 2. Partitioning of amino acids, amides and peptides in floral tissues. A, In the floral 599
receptacle, transporters of the families of Lysine Histidine Type (LHT), Amino Acid Permease 600
(AAP) and Oligo-Peptide Transporters (OPT) mediate the uptake of neutral (grey circles) and 601
acidic (grey circles with the minus sign) amino acids, neutral and basic (grey circles with the plus 602
sign) amino acids, and tetra- and penta-peptides (purple rectangles), respectively. Expression of 603
the same set of transporters at the base of the ovary suggests that they also mediate the uptake of 604
amino acids and peptides in the ovary. B, In sepals LHT, AAP, OPT, Proline Transporter (ProT) 605
and Cationic Amino acid Transporter (CAT) the latter mediating the transport of both neutral and 606
basic amino acids, are expressed in the cells surrounding the vasculature where they presumably 607
mediate xylem-phloem exchange and/or retrieval of leaked organic nitrogen. C, In petals, 608
plastidial CATs export Phe, Tyr and Trp to the cytoplasm, while Outer Envelope Plastidial 609
protein (OEP) imports amines (N) in the stroma. Mitochondrial Basic Amino acid Carriers 610
(BACs) import Arg in the mitochondrion (mt). Expression of LHT, AAP, OPT, ProT, and CAT 611
was also detected in the cells surrounding petal vasculature. Apoplasmically isolated tissues such 612
as the cells of the tapetum (D), developing pollen grains (E) and pollen tubes (F) express a vast 613
majority of different transporters. PTR-like Peptide Transporter (PTR) in pollen grains and pollen 614
tubes mediate the uptake of de- and tri-peptides. G, In nectar, the pool of amino acids and 615
peptides is depleted by colonizing yeasts and bacteria. 616
617
618
619
620
621
LITERATURE CITED 622
29
Aleklett K, Hart M, Shade A (2014) The microbial ecology of flowers: an emerging frontier in 623 phyllosphere research. Botany 92: 253-266 624
Aluri S, Büttner M (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar 625 glucose transporter 1 and its role in seed germination and flowering. Proceedings of the National 626 Academy of Sciences 104: 2537-2542 627
Amrad A, Moser M, Mandel T, de Vries M, Schuurink RC, Freitas L, Kuhlemeier C (2016) Gain and 628 loss of floral scent production through changes in structural genes during pollinator-mediated 629 speciation. Current Biology 26: 3303-3312 630
Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, Schwan MR, Walton A, Jones BM, Corby-631 Harris V (2013) Microbial ecology of the hive and pollination landscape: bacterial associates from 632 floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PloS One 8: 633 e83125 634
Aschan G, Pfanz H (2003) Non-foliar photosynthesis–a strategy of additional carbon acquisition. Flora-635 Morphology, Distribution, Functional Ecology of Plants 198: 81-97 636
Baker HG (1977) Non-sugar chemical constituents of nectar. Apidologie 8: 349-356 637 Belisle M, Peay KG, Fukami T (2012) Flowers as islands: spatial distribution of nectar-inhabiting 638
microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub. Microbial 639 Ecology 63: 711-718 640
Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S (2005) Genetic analysis of Arabidopsis GATA 641 transcription factor gene family reveals a nitrate‐inducible member important for chlorophyll 642 synthesis and glucose sensitivity. The Plant Journal 44: 680-692 643
Biancucci M, Mattioli R, Forlani G, Funck D, Costantino P, Trovato M (2015) Role of proline and 644 GABA in sexual reproduction of angiosperms. Frontiers in Plant Science 6 645
Bieleski RL (1993) Fructan hydrolysis drives petal expansion in the ephemeral daylily flower. Plant 646 Physiology 103: 213-219 647
Bieleski RL (1995) Onset of phloem export from senescent petals of daylily. Plant Physiology 109: 557-648 565 649
Boavida LC, Borges F, Becker JD, Feijó JA (2011) Whole genome analysis of gene expression reveals 650 coordinated activation of signaling and metabolic pathways during pollen-pistil interactions in 651 Arabidopsis. Plant Physiology 155: 2066-2080 652
Borghi M, Fernie AR, Schiestl FP, Bouwmeester HJ (2017) The Sexual Advantage of Looking, 653 Smelling, and Tasting Good: The Metabolic Network that Produces Signals for Pollinators. Trends 654 in Plant Science 655
Bradshaw Jr H, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator 656 shift in monkeyflowers. Nature 426: 176 657
Büttner M (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biology 12: 35-41 658 Canto A, Pérez R, Medrano M, Castellanos MC, Herrera CM (2007) Intra-plant variation in nectar 659
sugar composition in two Aquilegia species (Ranunculaceae): contrasting patterns under field and 660 glasshouse conditions. Annals of Botany 99: 653-660 661
Capron A, Gourgues M, Neiva LS, Faure J-E, Berger F, Pagnussat G, Krishnan A, Alvarez-Mejia C, 662 Vielle-Calzada J-P, Lee Y-R (2008) Maternal control of male-gamete delivery in Arabidopsis 663 involves a putative GPI-anchored protein encoded by the LORELEI gene. The Plant Cell 20: 3038-664 3049 665
Carrizo García C, Guarnieri M, Pacini E (2015) Carbohydrate metabolism before and after dehiscence 666 in the recalcitrant pollen of pumpkin (Cucurbita pepo L.). Plant Biology 17: 734-739 667
Carruthers JM, Cook SM, Wright GA, Osborne JL, Clark SJ, Swain JL, Haughton AJ (2017) Oilseed 668 rape (Brassica napus) as a resource for farmland insect pollinators: quantifying floral traits in 669 conventional varieties and breeding systems. GCB Bioenergy 670
Carter C, Shafir S, Yehonatan L, Palmer RG, Thornburg R (2006) A novel role for proline in plant 671 floral nectars. Naturwissenschaften 93: 72-79 672
Castro AJ, Clément C (2007) Sucrose and starch catabolism in the anther of Lilium during its 673 development: a comparative study among the anther wall, locular fluid and microspore/pollen 674 fractions. Planta 225: 1573-1582 675
Chen L-Q, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of sugars. Annual Review of 676 Biochemistry 84 677
Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J, Kim J-G, Underwood 678 W, Chaudhuri B (2010) Sugar transporters for intercellular exchange and nutrition of 679 pathogens. Nature 468: 527 680
Chen L-Q, Lin IW, Qu X-Q, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) 681 A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm 682 provides nutrition for the Arabidopsis embryo. The Plant Cell 27: 607-619 683
Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux 684 mediated by SWEET proteins as a key step for phloem transport. Science 335: 207-211 685
Chiang HH, Dandekar A (1995) Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh 686 during development and in response to desiccation. Plant, Cell and Environment 18: 1280-1290 687
30
Clare EL, Schiestl FP, Leitch AR, Chittka L (2013) The promise of genomics in the study of plant-688 pollinator interactions. Genome Biology 14: 207 689
Clarke A, Considine J, Ward R, Knox R (1977) Mechanism of pollination in Gladiolus: roles of the 690 stigma and pollen-tube guide. Annals of Botany 41: 15-20 691
Collier DE (1997) Changes in respiration, protein and carbohydrates of tulip tepals and Alstroemeria 692 petals during development. Journal of Plant Physiology 150: 446-451 693
Coruzzi GM (2003) Primary N-assimilation into amino acids in Arabidopsis. The Arabidopsis Book: e0010 694 Dancer JE, ap Rees T (1989) Effects of 2, 4-dinitrophenol and anoxia on the inorganic-pyrophosphate 695
content of the spadix of Arum maculatum and the root apices of Pisum sativum. Planta 178: 421-696 424 697
de Vega C, Herrera CM (2013) Microorganisms transported by ants induce changes in floral nectar 698 composition of an ant-pollinated plant. American Journal of Botany 100: 792-800 699
Dickinson DB (1965) Germination of lily pollen: respiration and tube growth. Science 150: 1818-1819 700 Dong Y, Li B, Aharoni A (2016) More than pictures: when MS imaging meets histology. Trends in Plant 701
Science 21: 686-698 702 Dresselhaus T, Franklin-Tong N (2013) Male–female crosstalk during pollen germination, tube growth 703
and guidance, and double fertilization. Molecular Plant 6: 1018-1036 704 Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity 705
in pollination. The Plant Cell 16: S84-S97 706 Elleman C, Franklin‐Tong V, Dickinson H (1992) Pollination in species with dry stigmas: the nature of 707
the early stigmatic response and the pathway taken by pollen tubes. New Phytologist 121: 413-708 424 709
Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell 710 surface? Plant Physiology 153: 403-419 711
Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete 712 promoters in Arabidopsis. Plant Physiology 138: 2124-2133 713
Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin I, Qu X-Q, Braun DM, Frommer WB (2015) SWEETs, 714 transporters for intracellular and intercellular sugar translocation. Current Opinion in Plant Biology 715 25: 53-62 716
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the 717 GABA shunt in plants. Trends in Plant Science 13: 14-19 718
Feng L, Frommer WB (2015) Structure and function of SemiSWEET and SWEET sugar transporters. 719 Trends in Biochemical Sciences 40: 480-486 720
Feuerstein A, Niedermeier M, Bauer K, Engelmann S, Hoth S, Stadler R, Sauer N (2010) 721 Expression of the AtSUC1 gene in the female gametophyte, and ecotype‐specific expression 722 differences in male reproductive organs. Plant Biology 12: 105-114 723
Foster J, Lee Y-H, Tegeder M (2008) Distinct expression of members of the LHT amino acid transporter 724 family in flowers indicates specific roles in plant reproduction. Sexual Plant Reproduction 21: 725 143-152 726
Franchi GG, Bellani L, Nepi M, Pacini E (1996) Types of carbohydrate reserves in pollen: localization, 727 systematic distribution and ecophysiological significance. Flora 191: 143-159 728
Franchi GG, Piotto B, Nepi M, Baskin CC, Baskin JM, Pacini E (2011) Pollen and seed desiccation 729 tolerance in relation to degree of developmental arrest, dispersal, and survival. Journal of 730 experimental botany 62:5267-5281 731
Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. 732 Environmental Microbiology Reports 4: 97-104 733
Gahrtz M, Schmelzer E, Stolz J, Sauer N (1996) Expression of the PmSUC1 sucrose carrier gene from 734 Plantago major L. is induced during seed development. The Plant Journal 9: 93-100 735
Gallagher MK, Campbell DR (2017). Shifts in water availability mediate plant–pollinator interactions. 736 New Phytologist 215: 792–802 737
Gass N, Glagotskaia T, Mellema S, Stuurman J, Barone M, Mandel T, Roessner-Tunali U, 738 Kuhlemeier C (2005) Pyruvate decarboxylase provides growing pollen tubes with a competitive 739 advantage in petunia. The Plant Cell 17: 2355-2368 740
Gaufichon L, Marmagne A, Belcram K, Yoneyama T, Sakakibara Y, Hase T, Grandjean O, Gilles C, 741 Citerne S, Boutet‐Mercey S (2017) ASN1‐encoded asparagine synthetase in floral organs 742 contributes to nitrogen filling in Arabidopsis seeds. The Plant Journal 91: 371–393 743
Ge YX, Angenent GC, Wittich PE, Peters J, Franken J, Busscher M, Zhang LM, Dahlhaus E, Kater 744 MM, Wullems GJ (2000) NEC1, a novel gene, highly expressed in nectary tissue of Petunia 745 hybrida. The Plant Journal 24: 725-734 746
Geigenberger P, Stitt M (1991) A futile cycle of sucrose synthesis and degradation is involved in 747 regulating partitioning between sucrose, starch and respiration in cotyledons of germinating 748 Ricinus communis L seedlings when phloem transport is inhibited. Planta 185: 81-90 749
Gisel A, Hempel FD, Barella S, Zambryski P (2002) Leaf-to-shoot apex movement of symplastic tracer 750 is restricted coincident with flowering in Arabidopsis. Proceedings of the National Academy of 751 Sciences 99: 1713-1717 752
31
Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility 753 in plants by metabolic engineering of the carbohydrate supply. Proceedings of the National 754 Academy of Sciences 98: 6522-6527 755
Goetz M, Guivarćh A, Hirsche J, Bauerfeind MA, González M-C, Hyun TK, Eom SH, Chriqui D, 756 Engelke T, Großkinsky DK (2017) Metabolic control of tobacco pollination by sugars and 757 invertases. Plant Physiology 173: 984-997 758
Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57: 761-761 780 762
Guan M, Møller IS, Schjørring JK (2014) Two cytosolic glutamine synthetase isoforms play specific 763 roles for seed germination and seed yield structure in Arabidopsis. Journal of Experimental 764 Botany 66: 203-212 765
Guan Y-F, Huang X-Y, Zhu J, Gao J-F, Zhang H-X, Yang Z-N (2008) RUPTURED POLLEN GRAIN1, a 766 member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of 767 microspores in Arabidopsis. Plant Physiology 147: 852-863 768
Hafidh S, Fíla J, Honys D (2016) Male gametophyte development and function in angiosperms: a 769 general concept. Plant Reproduction 29: 31-51 770
Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and 771 variation in pollen quality in British herbaceous plants. Functional Ecology 22: 592-598 772
Hedhly A, Vogler H, Schmid MW, Pazmino D, Gagliardini V, Santelia D, Grossniklaus U (2016) 773 Starch turnover and metabolism during flower and early embryo development. Plant Physiology: 774 pp. 00916.02016 775
Heil M (2011) Nectar: generation, regulation and ecological functions. Trends in Plant Science 16: 191-776 200 777
Herrera CM, García IM, Pérez R (2008) INVISIBLE FLORAL LARCENIES: MICROBIAL COMMUNITIES 778 DEGRADE FLORAL NECTAR OF BUMBLE BEE‐POLLINATED PLANTS. Ecology 89: 2369-2376 779
Hew C, Yip K (1991) Respiration of orchid flower mitochondria. Botanical Gazette 152: 289-295 780 Higashiyama T, Yang W-c (2017) Gametophytic pollen tube guidance: attractant peptides, gametic 781
controls, and receptors. Plant Physiology 173: 112-121 782 Hirsche J, Engelke T, Völler D, Götz M, Roitsch T (2009) Interspecies compatibility of the anther 783
specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile 784 plants. Theoretical and Applied Genetics 118: 235-245 785
Ho L, Nichols R (1975) The role of phloem transport in the translocation of sucrose along the stem of 786 carnation cut flowers. Annals of Botany 39: 439-446 787
Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell'Olivo A, Arnold M, 788 Kuhlemeier C (2007) Single gene–mediated shift in pollinator attraction in Petunia. The Plant 789 Cell 19: 779-790 790
Hoekstra F, Crowe L, Crowe J (1989) Differential desiccation sensitivity of corn and Pennisetum pollen 791 linked to their sucrose contents. Plant, Cell and Environment 12: 83-91 792
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent 793 protein in the phloem and symplastic unloading of the protein into sink tissues. The Plant Cell 11: 794 309-322 795
Ivanov A, Kameka A, Pajak A, Bruneau L, Beyaert R, Hernández-Sebastià C, Marsolais F (2012) 796 Arabidopsis mutants lacking asparaginases develop normally but exhibit enhanced root inhibition 797 by exogenous asparagine. Amino Acids 42: 2307-2318 798
Jiao J, Mizukami AG, Sankaranarayanan S, Yamguchi J, Itami K, Higashiyama T (2016) Structure-799 Activity Relation of AMOR Sugar Molecule That Activates Pollen-Tubes for Ovular Guidance. Plant 800 Physiology 173: 354-363. 801
Johnson MA, von Besser K, Zhou Q, Smith E, Aux G, Patton D, Levin JZ, Preuss D (2004) 802 Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168: 971-982 803
Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter‐tasting nectar functions as a filter of flower 804 visitors in a bird‐pollinated plant. Ecology 87: 2709-2716 805
Jones-Rhoades MW, Borevitz JO, Preuss D (2007) Genome-wide expression profiling of the 806 Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genetics 3: 807 e171 808
Junker RR, Keller A (2015) Microhabitat heterogeneity across leaves and flower organs promotes 809 bacterial diversity. FEMS Microbiology Ecology 91: fiv097 810
Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N (2011) Composition of epiphytic 811 bacterial communities differs on petals and leaves. Plant Biology 13: 918-924 812
Junker RR, Romeike T, Keller A, Langen D (2014) Density-dependent negative responses by 813 bumblebees to bacteria isolated from flowers. Apidologie 45: 467-477 814
Karapanos I, Akoumianakis K, Olympios C, Passam HC (2010) Tomato pollen respiration in relation 815 to in vitro germination and pollen tube growth under favourable and stress-inducing 816 temperatures. Sexual Plant Reproduction 23: 219-224 817
32
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites 818 on floral visitors of Nicotiana attenuata. The Plant Journal 49: 840-854 819
Khan MI, Giridhar P (2015) Plant betalains: chemistry and biochemistry. Phytochemistry 117: 267-295 820 Kishor PBK, Kumari PH, Sunita M, Sreenivasulu N (2015) Role of proline in cell wall synthesis and 821
plant development and its implications in plant ontogeny. Frontiers in Plant Science 6 822 Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E, Guerin PM, Kuhlemeier C (2011) 823
Pollinator choice in Petunia depends on two major genetic loci for floral scent production. Current 824 Biology 21: 730-739 825
Klepek Y-S, Geiger D, Stadler R, Klebl F, Landouar-Arsivaud L, Lemoine R, Hedrich R, Sauer N 826 (2005) Arabidopsis POLYOL TRANSPORTER5, a new member of the monosaccharide transporter-827 like superfamily, mediates H+-symport of numerous substrates, including myo-inositol, glycerol, 828 and ribose. The Plant Cell 17: 204-218 829
Klepek Y-S, Volke M, Konrad KR, Wippel K, Hoth S, Hedrich R, Sauer N (2009) Arabidopsis thaliana 830 POLYOL/MONOSACCHARIDE TRANSPORTERS 1 and 2: fructose and xylitol/H+ symporters in 831 pollen and young xylem cells. Journal of experimental botany 61: 537-550 832
Knoch E, Dilokpimol A, Geshi N (2014) Arabinogalactan proteins: focus on carbohydrate active 833 enzymes. Frontiers in Plant Science 5 834
Konar R, Linskens H (1966) Physiology and biochemistry of the stigmatic fluid of Petunia hybrida. Planta 835 71: 372-387 836
Kram BW, Xu WW, Carter CJ (2009) Uncovering the Arabidopsis thaliana nectary transcriptome: 837 investigation of differential gene expression in floral nectariferous tissues. BMC Plant Biology 9: 838 92 839
Labarca C, Kroh M, Loewus F (1970) The Composition of Stigmatic Exudate from Lilium longiflorum 840 Labeling Studies with Myo-inositol, d-Glucose, and l-Proline. Plant Physiology 46: 150-156 841
Labarca C, Loewus F (1972) The nutritional role of pistil exudate in pollen tube wall formation in Lilium 842 longiflorum I. Utilization of injected stigmatic exudate. Plant Physiology 50: 7-14 843
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and 844 nitrogen between source and sink. Annu. Rev. Plant Biol. 55: 341-372 845
Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary 846 cell wall architecture. Plant Physiology 156: 11-19 847
Lauxmann MA, Annunziata MG, Brunoud G, Wahl V, Koczut A, Burgos A, Olas JJ, Maximova E, 848 Abel C, Schlereth A (2016) Reproductive failure in Arabidopsis thaliana under transient 849 carbohydrate limitation: flowers and very young siliques are jettisoned and the meristem is 850 maintained to allow successful resumption of reproductive growth. Plant, Cell and Environment 851 39: 745-767 852
Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride 853 R, Horvath S (2010) Global analysis of gene activity during Arabidopsis seed development and 854 identification of seed-specific transcription factors. Proceedings of the National Academy of 855 Sciences 107: 8063-8070 856
Le Roy K, Vergauwen R, Struyf T, Yuan S, Lammens W, Mátrai J, De Maeyer M, Van den Ende W 857 (2013) Understanding the role of defective invertases in plants: tobacco Nin88 fails to degrade 858 sucrose. Plant Physiology 161: 1670-1681 859
Lee CB, Kim S, McClure B (2009) A pollen protein, NaPCCP, that binds pistil arabinogalactan proteins 860 also binds phosphatidylinositol 3-phosphate and associates with the pollen tube endomembrane 861 system. Plant Physiology 149: 791-802 862
Lee CB, Swatek KN, McClure B (2008) Pollen proteins bind to the C-terminal domain of Nicotiana alata 863 pistil arabinogalactan proteins. Journal of Biological Chemistry 283: 26965-26973 864
Lenaerts M, Pozo MI, Wäckers F, Van den Ende W, Jacquemyn H, Lievens B (2016) Impact of 865 microbial communities on floral nectar chemistry: potential implications for biological control of 866 pest insects. Basic and Applied Ecology 17: 189-198 867
Lin IW, Sosso D, Chen L-Q, Gase K, Kim S-G, Kessler D, Klinkenberg PM, Gorder MK, Hou B-H, 868 Qu X-Q (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter 869 SWEET9. Nature 508: 546 870
Liu G, Ren G, Guirgis A, Thornburg RW (2009) The MYB305 transcription factor regulates expression of 871 nectarin genes in the ornamental tobacco floral nectary. The Plant Cell 21: 2672-2687 872
Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. 873 Annual Review of Plant Biology 63: 73-105 874
Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooper BR, Rhodes D, Pichersky E, 875 Dudareva N (2010) RNAi suppression of Arogenate Dehydratase1 reveals that phenylalanine is 876 synthesized predominantly via the arogenate pathway in petunia petals. The Plant Cell 22: 832-877 849 878
Maeda H, Yoo H, Dudareva N (2011) Prephenate aminotransferase directs plant phenylalanine 879 biosynthesis via arogenate. Nature Chemical Biology 7: 19-21 880
Mascarenhas JP (1970) A new intermediate in plant cell wall synthesis. Biochemical and Biophysical 881 Research Communications 41: 142-149 882
Mascarenhas JP (1989) The male gametophyte of flowering plants. The Plant Cell 1: 657 883
33
Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004) Wounding enhances 884 expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. 885 Plant Physiology 134: 684-693 886
Meyer S, Melzer M, Truernit E, HuÈmmer C, Besenbeck R, Stadler R, Sauer N (2000) AtSUC3, a 887 gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the 888 vascular tissue and in a carpel cell layer. The Plant Journal 24: 869-882 889
Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant, 890 Cell and Environment 37: 1936-1949 891
Muhlemann JK, Maeda H, Chang C-Y, San Miguel P, Baxter I, Cooper B, Perera MA, Nikolau BJ, 892 Vitek O, Morgan JA (2012) Developmental changes in the metabolic network of snapdragon 893 flowers. PLoS One 7: e40381 894
Müller GL, Drincovich MF, Andreo CS, Lara MV (2010) Role of photosynthesis and analysis of key 895 enzymes involved in primary metabolism throughout the lifespan of the tobacco flower. Journal of 896 Experimental Botany 61: 3675-3688 897
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182: 898 31-48 899
Nepi M (2014) Beyond nectar sweetness: the hidden ecological role of non‐protein amino acids in nectar. 900 Journal of Ecology 102: 108-115 901
Nepi M (2017) New perspectives in nectar evolution and ecology: simple alimentary reward or a complex 902 multiorganism interaction? Acta Agrobotanica 70 903
Nepi M, Franchi G, Padni E (2001) Pollen hydration status at dispersal: cytophysiological features and 904 strategies. Protoplasma 216: 171 905
Nepi M, Soligo C, Nocentini D, Abate M, Guarnieri M, Cai G, Bini L, Puglia M, Bianchi L, Pacini E 906 (2012) Amino acids and protein profile in floral nectar: much more than a simple reward. Flora-907 Morphology, Distribution, Functional Ecology of Plants 207: 475-481 908
Nguyen-Quoc B, Foyer CH (2001). A role for 'futile cycles' involving invertase and sucrose synthase in 909 sucrose metabolism of tomato fruit. Journal of Experimental Botany 52: 881-889. 910
U-I, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator 913 GPT1 is essential for pollen maturation and embryo sac development. The Plant Cell 17: 760-775 914
Nørholm MH, Nour-Eldin HH, Brodersen P, Mundy J, Halkier BA (2006) Expression of the 915 Arabidopsis high‐affinity hexose transporter STP13 correlates with programmed cell death. FEBS 916 Letters 580: 2381-2387 917
Noutsos C, Perera AM, Nikolau BJ, Seaver SM, Ware DH (2015) Metabolomic Profiling of the Nectars 918 of Aquilegia pubescens and A. Canadensis. PloS One 10: e0124501 919
O'Neill SD (1997) Pollination regulation of flower development. Annual review of plant biology 48: 547-920 574 921
Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, 922 Mizukami A, Susaki D (2009) Defensin-like polypeptide LUREs are pollen tube attractants 923 secreted from synergid cells. Nature 458: 357-361 924
Owen CR, Bradshaw H (2011) Induced mutations affecting pollinator choice in Mimulus lewisii 925 (Phrymaceae). Arthropod-Plant Interactions 5: 235 926
Pacini E, Franchi G, Hesse M (1985) The tapetum: Its form, function, and possible phylogeny 927 inEmbryophyta. Plant Systematics and Evolution 149: 155-185 928
Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, 929 presentation, and dispersal: a short review. Protoplasma 228: 73-77 930
Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by 931 POP2, an Arabidopsis gene that controls GABA levels. Cell 114: 47-59 932
Pélabon C, Hennet L, Strimbeck R, Johnson H, Armbruster WS (2015) Blossom colour change after 933 pollination provides carbon for developing seeds. Functional Ecology 29: 1137-1143 934
Persia D, Cai G, Del Casino C, Faleri C, Willemse MT, Cresti M (2008) Sucrose synthase is associated 935 with the cell wall of tobacco pollen tubes. Plant Physiology 147: 1603-1618 936
Petanidou T, Van Laere A, N Ellis W, Smets E (2006) What shapes amino acid and sugar composition 937 in Mediterranean floral nectars? Oikos 115: 155-169 938
Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Critical 939 Reviews in Plant Sciences 25: 159-198 940
Pozo MI, Herrera CM, Lachance MA, Verstrepen K, Lievens B, Jacquemyn H (2016) Species 941 coexistence in simple microbial communities: unravelling the phenotypic landscape of co‐942 occurring Metschnikowia species in floral nectar. Environmental Microbiology 18: 1850-1862 943
Pressman E, Shaked R, Shen S, Altahan L, Firon N (2012) Variations in carbohydrate content and 944 sucrose-metabolizing enzymes in tomato (Solanum lycopersicum L.) stamen parts during pollen 945 maturation. Am J Plant Sci 3: 252-260 946
Reinders A, Panshyshyn JA, Ward JM (2005) Analysis of transport activity of Arabidopsis sugar alcohol 947 permease homolog AtPLT5. Journal of Biological Chemistry 280: 1594-1602 948
34
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen 949 compounds in plants. FEBS Letters 581: 2281-2289 950
Rosen WG, Thomas HR (1970) Secretory cells of lily pistils. I. Fine structure and function. American 951 Journal of Botany: 1108-1114 952
Rottmann T, Zierer W, Subert C, Sauer N, Stadler R (2016) STP10 encodes a high-affinity 953 monosaccharide transporter and is induced under low-glucose conditions in pollen tubes of 954 Arabidopsis. Journal of Experimental Botany 67: 2387-2399 955
Rounds CM, Winship LJ, Hepler PK (2011) Pollen tube energetics: respiration, fermentation and the 956 race to the ovule. AoB Plants 2011: plr019 957
Roy R, Schmitt AJ, Thomas JB, Carter CJ (2017) Nectar biology: from molecules to ecosystems. Plant 958 Science 959
Ruan Y-L, Jin Y, Yang Y-J, Li G-J, Boyer JS (2010) Sugar input, metabolism, and signaling mediated 960 by invertase: roles in development, yield potential, and response to drought and heat. Molecular 961 Plant 3: 942-955 962
Sassen M (1974) The stylar transmitting tissue. Plant Biology 23: 99-108 963 Sauer N, Friedländer K, Gräml-Wicke U (1990) Primary structure, genomic organization and 964
heterologous expression of a glucose transporter from Arabidopsis thaliana. The EMBO Journal 9: 965 3045 966
Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M, Klebl F (2004) AtSUC8 and AtSUC9 encode 967 functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode 968 aberrant proteins in different Arabidopsis ecotypes. The Plant Journal 40: 120-130 969
Sauer N, Stolz J (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression 970 and characterization in baker's yeast and identification of the histidine‐tagged protein. The Plant 971 Journal 6: 67-77 972
Schaeffer RN, Irwin RE (2014) Yeasts in nectar enhance male fitness in a montane perennial herb. 973 Ecology 95: 1792-1798 974
Schaeffer RN, Vannette RL, Irwin RE (2015) Nectar yeasts in Delphinium nuttallianum 975 (Ranunculaceae) and their effects on nectar quality. Fungal Ecology 18: 100-106 976
Schneider S, Hulpke S, Schulz A, Yaron I, Höll J, Imlau A, Schmitt B, Batz S, Wolf S, Hedrich R 977 (2012) Vacuoles release sucrose via tonoplast‐localised SUC4‐type transporters. Plant Biology 14: 978 325-336 979
Schneider S, Schneidereit A, Konrad KR, Hajirezaei M-R, Gramann M, Hedrich R, Sauer N (2006) 980 Arabidopsis INOSITOL TRANSPORTER4 mediates high-affinity H+ symport of myoinositol across 981 the plasma membrane. Plant Physiology 141: 565-577 982
Schneider S, Schneidereit A, Udvardi P, Hammes U, Gramann M, Dietrich P, Sauer N (2007) 983 Arabidopsis INOSITOL TRANSPORTER2 mediates H+ symport of different inositol epimers and 984 derivatives across the plasma membrane. Plant Physiology 145: 1395-1407 985
Schneidereit A, Scholz-Starke J, Büttner M (2003) Functional characterization and expression 986 analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. 987 Plant Physiology 133: 182-190 988
Schneidereit A, Scholz-Starke J, Sauer N, Büttner M (2005) AtSTP11, a pollen tube-specific 989 monosaccharide transporter in Arabidopsis. Planta 221: 48-55 990
Scholz-Starke J, Büttner M, Sauer N (2003) AtSTP6, a new pollen-specific H+-monosaccharide 991 symporter from Arabidopsis. Plant Physiology 131: 70-77 992
Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) 993 LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. 994 The Plant Cell 11: 377-391 995
Sedio BE (2017) Recent breakthroughs in metabolomics promise to reveal the cryptic chemical traits that 996 mediate plant community composition, character evolution and lineage diversification. New 997 Phytologist 214: 952-958 998
Seymour RS (1999) Pattern of respiration by intact inflorescences of the thermogenic arum lily 999 Philodendron selloum. Journal of Experimental Botany 50: 845-852 1000
Sheehan H, Moser M, Klahre U, Esfeld K, Dell'Olivo A, Mandel T, Metzger S, Vandenbussche M, 1001 Freitas L, Kuhlemeier C (2016) MYB-FL controls gain and loss of floral UV absorbance, a key 1002 trait affecting pollinator preference and reproductive isolation. Nature genetics 48: 159 1003
Singh MB, Knox RB (1984) Invertases of Lilium pollen Characterization and activity during in vitro 1004 germination. Plant Physiology 74: 510-515 1005
Sivitz AB, Reinders A, Ward JM (2008) Arabidopsis sucrose transporter AtSUC1 is important for pollen 1006 germination and sucrose-induced anthocyanin accumulation. Plant Physiology 147: 92-100 1007
Sklensky DE, Davies PJ (2011) Resource partitioning to male and female flowers of Spinacia oleracea L. 1008 in relation to whole-plant monocarpic senescence. Journal of Experimental Botany 62: 4323-4336 1009
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell and Environment 1010 30: 1126-1149 1011
Sosso D, Luo D, Li Q-B, Sasse J, Yang J, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS 1012 (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose 1013 transport. Nature Genetics 47: 1489 1014
35
Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals 1015 post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis 1016 seeds and embryos. Plant Physiology 139: 701-712 1017
Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the 1018 osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. The Plant 1019 Journal 19: 269-278 1020
Sun M-X, Huang X-Y, Yang J, Guan Y-F, Yang Z-N (2013) Arabidopsis RPG1 is important for primexine 1021 deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. 1022 Plant Reproduction 26: 83-91 1023
Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible 1024 pollen tube attractants in Arabidopsis. PLoS Biology 10: e1001449 1025
Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and 1026 carotenoids. The Plant Journal 54: 733-749 1027
Tegeder M (2012) Transporters for amino acids in plant cells: some functions and many unknowns. 1028 Current Opinion in Plant Biology 15: 315-321 1029
Tegeder M, Rentsch D (2010) Uptake and partitioning of amino acids and peptides. Molecular Plant 3: 1030 997-1011 1031
Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. Journal of 1032 Experimental Botany 54: 1127-1132 1033
Truernit E, Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene 1034 directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading 1035 by SUC2. Planta 196: 564-570 1036
Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink-specific and stress-regulated 1037 Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter 1038 by wounding, elicitors, and pathogen challenge. The Plant Cell 8: 2169-2182 1039
Truernit E, Stadler R, Baier K, Sauer N (1999) A male gametophyte‐specific monosaccharide 1040 transporter inArabidopsis. The Plant Journal 17: 191-201 1041
Tsanakas GF, Manioudaki ME, Economou AS, Kalaitzis P (2014) De novo transcriptome analysis of 1042 petal senescence in Gardenia jasminoides Ellis. BMC Genomics 15: 554 1043
van Doorn WG, Kamdee C (2014) Flower opening and closure: an update. Journal of Experimental 1044 Botany 65: 5749-5757 1045
van Doorn WG, van Meeteren U (2003) Flower opening and closure: a review. Journal of Experimental 1046 Botany 54: 1801-1812 1047
Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014) How 1048 does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS One 9: 1049 e86209 1050
Vanderplanck M, Vereecken NJ, Grumiau L, Esposito F, Lognay G, Wattiez R, Michez D (2017) The 1051 importance of pollen chemistry in evolutionary host shifts of bees. Scientific Reports 7 1052
Vannette RL, Fukami T (2016) Nectar microbes can reduce secondary metabolites in nectar and alter 1053 effects on nectar consumption by pollinators. Ecology 97: 1410-1419 1054
Vannette RL, Gauthier M-PL, Fukami T (2013) Nectar bacteria, but not yeast, weaken a plant–1055 pollinator mutualism. Proceedings of the Royal Society of London B: Biological Sciences 280: 1056 20122601 1057
Wagstaff C, Yang TJ, Stead AD, Buchanan‐Wollaston V, Roberts JA (2009) A molecular and 1058 structural characterization of senescing Arabidopsis siliques and comparison of transcriptional 1059 profiles with senescing petals and leaves. The Plant Journal 57: 690-705 1060
Wang L, Ruan Y-L (2016) Critical roles of vacuolar invertase in floral organ development and male and 1061 female fertilities are revealed through characterization of GhVIN1-RNAi cotton plants. Plant 1062 Physiology 171: 405-423 1063
Weber H, Borisjuk L, Wobus U (1997) Sugar import and metabolism during seed development. Trends 1064 in Plant Science 2: 169-174 1065
Weiner CN, Hilpert A, Werner M, Linsenmair KE, Blüthgen N (2010) Pollen amino acids and flower 1066 specialisation in solitary bees. Apidologie 41: 476-487 1067
Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB, Ward JM (2000) A new 1068 subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate 1069 sieve elements of plants. The Plant Cell 12: 1345-1355 1070
Weiss D, Schönfeld M, Halevy AH (1988) Photosynthetic activities in the Petunia corolla. Plant 1071 Physiology 87: 666-670 1072
Werner D, Gerlitz N, Stadler R (2011) A dual switch in phloem unloading during ovule development in 1073 Arabidopsis. Protoplasma 248: 225-235 1074
Widhalm JR, Gutensohn M, Yoo H, Adebesin F, Qian Y, Guo L, Jaini R, Lynch JH, McCoy RM, 1075 Shreve JT (2015) Identification of a plastidial phenylalanine exporter that influences flux 1076 distribution through the phenylalanine biosynthetic network. Nature Communications 6 1077
Wiesen LB, Bender RL, Paradis T, Larson A, Perera MAD, Nikolau BJ, Olszewski NE, Carter CJ 1078 (2016) A Role for GIBBERELLIN 2-OXIDASE6 and Gibberellins in Regulating Nectar Production. 1079 Molecular Plant 9: 753-756 1080
36
Ylstra B, Garrido D, Busscher J, van Tunen AJ (1998) Hexose transport in growing petunia pollen 1081 tubes and characterization of a pollen-specific, putative monosaccharide transporter. Plant 1082 Physiology 118: 297-304 1083
Yoo H, Widhalm JR, Qian Y, Maeda H, Cooper BR, Jannasch AS, Gonda I, Lewinsohn E, Rhodes 1084 D, Dudareva N (2013) An alternative pathway contributes to phenylalanine biosynthesis in 1085 plants via a cytosolic tyrosine: phenylpyruvate aminotransferase. Nature Communications 4: 1086 2833 1087
Yuan Y-W, Byers KJ, Bradshaw H (2013) The genetic control of flower–pollinator specificity. Current 1088 opinion in plant biology 16: 422-428 1089
Zhou Y, Li M, Zhao F, Zha H, Yang L, Lu Y, Wang G, Shi J, Chen J (2016) Floral Nectary Morphology 1090 and Proteomic Analysis of Nectar of Liriodendron tulipifera Linn. Frontiers in Plant Science 7 1091
1092
1093
sucrose
glucose fructose
starch
SWEET
SUC/SUT
STP
PMT
INT
VGT1
yeasts/bacteria
oil polysaccharides
A
B
C
D
E
F
Terminal
Phloem
cwINV
Apoplasm Receptacle Filament
cwINV
B A
amyloplast
Anther Wall Tapetum
C
Loculus Pollen Grain
D
vacuole
amyloplast
Pollen
Tube
Transmitting tissue
E
Nectary parenchyma
F
cwINV
Nectar Apoplasm
amyloplast
cwINV ♂♀
VIN ♀
♂♀ male/female
amyloplast
GPT1
SUS +
UDP
cwINV
UDP
SUS +
UDP
cwINV
UDP
SUS +
UDP
cwINV
UDP
SPS
P
UDP P
SPP + H2O
UDP +
Pi
P
SPS
P
UDP P
SPP + H2O
UDP +
Pi
P
+ Pi
Figure 1. Sugar partitioning in floral tissues. A, Unload of sucrose from the terminal phloem: SUGAR WILL EVENTUALLY BE
TRANSPORTED TRANSPORTERS (SWEET) are likely been involved in the process. Cell wall invertase (cwINV) enzymes in the apoplasmic
space hydrolyze sucrose to glucose and fructose. SUCROSE TRANSPORTERS (SUTs) alternatively called SUCROSE CARRIERs (SUCs)
and SUGAR TRANSPORTER PROTEINS (STPs) carry sucrose and hexose across the plasma membrane of the receptacle cells where
carbohydrates are stored as transitory starch. B, In the receptacle, sucrose and hexoses are symplasmically transferred to the anthers. C,
cwINVs and sucrose synthases (SUS) hydrolyze sucrose to hexoses, which are transported in the tapetum by SUC/SUT and STP
transporters. In the tapetum while it develops, carbohydrates are stored as transitory starch, which is later converted to sucrose by the
combined activity of sucrose phosphate synthases (SPS) and sucrose phosphate phosphatase (SPP). D, Pollen grains are apoplasmically
isolated and take up sucrose and hexoses via SUC/SUT and STP proteins. In developing pollen grains glucose-6-phosphate is transported
across the membrane of amyloplasts by GLUCOSE PHOSPHATE TRANSPORTER 1. Later during development, glucose released by the
amyloplasts is internalized in the vacuole by the activity of VACUOLAR GLUCOSE TRANSPORTER 1 (VGT1) and utilized for sucrose
synthesis. Depending upon the species, droplets of lipids may also accumulate in mature pollen grains. E, Pollen tube elongation is fuelled by
sugars secreted by the transmitting tissue. Hexoses are released in the transmitting tissue by the combined activity of cwINV of pollen grain
(♂) and stigma (♀), and by stigma specific vacuolar invertases (VIN). F, SUC/SUT and STP in the cells of the nectary parenchyma take up
sucrose and hexoses that are stored as starch granules. Before anthesis, transitory starch is converted to sucrose that is exported by SWEET
proteins to the apoplasmic space for nectar secretion. Here, cwINVs hydrolyze sucrose to fructose and glucose. Alternatively, fermentation
reactions carried out by colonizing yeasts and bacteria modify the sugar composition of nectar by releasing hexoses. Sometimes, the
production of a mucous matrix of polysaccharides has also been observed.
Figure 2. Partitioning of amino acids, amides and peptides in floral tissues. A, In the floral receptacle, transporters of the families of Lysine
Histidine Type (LHT), Amino Acid Permease (AAP) and Oligo-Peptide Transporters (OPT) mediate the uptake of neutral (grey circles) and
acidic (grey circles with the minus sign) amino acids, neutral and basic (grey circles with the plus sign) amino acids, and tetra- and penta-
peptides (purple rectangles), respectively. Expression of the same set of transporters at the base of the ovary suggests that they also
mediate the uptake of amino acids and peptides in the ovary. B, In sepals LHT, AAP, OPT, Proline Transporter (ProT) and Cationic Amino
acid Transporter (CAT) the latter mediating the transport of both neutral and basic amino acids, are expressed in the cells surrounding the
vasculature where they presumably mediate xylem-phloem exchange and/or retrieval of leaked organic nitrogen. C, In petals, plastidial CATs
export Phe, Tyr and Trp to the cytoplasm, while Outer Envelope Plastidial protein (OEP) imports amines (N) in the stroma. Mitochondrial
Basic Amino acid Carriers (BACs) import Arg in the mitochondrion (mt). Expression of LHT, AAP, OPT, ProT, and CAT was also detected in
the cells surrounding petal vasculature. Apoplasmically isolated tissues such as the cells of the tapetum (D), developing pollen grains (E) and
pollen tubes (F) express a vast majority of different transporters. PTR-like Peptide Transporter (PTR) in pollen grains and pollen tubes
mediate the uptake of de- and tri-peptides. G, In nectar, the pool of amino acids and peptides is depleted by colonizing yeasts and bacteria.
A
D
E
F
G
A
LHT
ProT
AAP
OPT
BAC
OEP
PTR
CAT
neutral amino acids
basic amino acids +
acidic amino acids -
amine
yeasts/bacteria
Pro
Phe/Tyr/Trp
peptide
Loculus Pollen Grain
E
B
C
Apoplasm Receptacle Ovary
- -
Petal Vasculature
-
C mt
Arg
+ +
+ -
+ + -
Sepal
B
Vasculature
- -
+ +
+ - -
+
+ - +
-
Anther Wall Tapetum
D
- -
+ +
-
- +
+
-
+
-
+
Pollen
Tube
Transmitting tissue
F G
Nectar
- - -
+ +
+ +
+
-
-
-
-
plastid
plastid
mt
Arg
N ..
N ..
N ..
N ..
N ..
ADVANCES
• The functional coupling of cwINV of the pollen
tube and transmitting tissue supports tube
elongation and successful fertilization.
• The sugar moiety of AGPs enables pollen
response to LURE.
• Asparagine synthesis in flowers is supported by
ASN1, which provides asparagine for embryo
development.
• SWEET9 regulates nectar secretion.
OUTSTANDING QUESTIONS
• In which measure is floral central metabolism
self-sustained or supported by carbon and
nitrogen fluxes from source tissues?
• How is floral central metabolism
transcriptionally and posttranscriptionally
regulated?
• What is the influence of environmental cues on
floral central metabolism and how does this
influence flower-pollinator interactions and
ultimately fruit and seed yield?
• What regulates the secretion of amino acids and
proteins into nectar?
• How do developmental changes in the
metabolism of one floral organ influence the
metabolism of others?
Parsed CitationsAleklett K, Hart M, Shade A (2014) The microbial ecology of flowers: an emerging frontier in phyllosphere research. Botany 92: 253-266
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Aluri S, Büttner M (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and itsrole in seed germination and flowering. Proceedings of the National Academy of Sciences 104: 2537-2542
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Amrad A, Moser M, Mandel T, de Vries M, Schuurink RC, Freitas L, Kuhlemeier C (2016) Gain and loss of floral scent productionthrough changes in structural genes during pollinator-mediated speciation. Current Biology 26: 3303-3312
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, Schwan MR, Walton A, Jones BM, Corby-Harris V (2013) Microbial ecology ofthe hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apismellifera). PloS One 8: e83125
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Aschan G, Pfanz H (2003) Non-foliar photosynthesis–a strategy of additional carbon acquisition. Flora-Morphology, Distribution,Functional Ecology of Plants 198: 81-97
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Baker HG (1977) Non-sugar chemical constituents of nectar. Apidologie 8: 349-356Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Belisle M, Peay KG, Fukami T (2012) Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulusaurantiacus, a hummingbird-pollinated shrub. Microbial Ecology 63: 711-718
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S (2005) Genetic analysis of Arabidopsis GATA transcription factor gene familyreveals a nitrate inducible member important for chlorophyll synthesis and glucose sensitivity. The Plant Journal 44: 680-692
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Biancucci M, Mattioli R, Forlani G, Funck D, Costantino P, Trovato M (2015) Role of proline and GABA in sexual reproduction ofangiosperms. Frontiers in Plant Science 6
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bieleski RL (1993) Fructan hydrolysis drives petal expansion in the ephemeral daylily flower. Plant Physiology 103: 213-219Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bieleski RL (1995) Onset of phloem export from senescent petals of daylily. Plant Physiology 109: 557-565Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Boavida LC, Borges F, Becker JD, Feijó JA (2011) Whole genome analysis of gene expression reveals coordinated activation ofsignaling and metabolic pathways during pollen-pistil interactions in Arabidopsis. Plant Physiology 155: 2066-2080
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Borghi M, Fernie AR, Schiestl FP, Bouwmeester HJ (2017) The Sexual Advantage of Looking, Smelling, and Tasting Good: TheMetabolic Network that Produces Signals for Pollinators. Trends in Plant Science
Pubmed: Author and TitleCrossRef: Author and Title
Google Scholar: Author Only Title Only Author and Title
Bradshaw Jr H, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature426: 176
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Büttner M (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biology 12: 35-41Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Canto A, Pérez R, Medrano M, Castellanos MC, Herrera CM (2007) Intra-plant variation in nectar sugar composition in two Aquilegiaspecies (Ranunculaceae): contrasting patterns under field and glasshouse conditions. Annals of Botany 99: 653-660
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Capron A, Gourgues M, Neiva LS, Faure J-E, Berger F, Pagnussat G, Krishnan A, Alvarez-Mejia C, Vielle-Calzada J-P, Lee Y-R (2008)Maternal control of male-gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. ThePlant Cell 20: 3038-3049
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Carrizo García C, Guarnieri M, Pacini E (2015) Carbohydrate metabolism before and after dehiscence in the recalcitrant pollen ofpumpkin (Cucurbita pepo L.). Plant Biology 17: 734-739
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Carruthers JM, Cook SM, Wright GA, Osborne JL, Clark SJ, Swain JL, Haughton AJ (2017) Oilseed rape (Brassica napus) as a resourcefor farmland insect pollinators: quantifying floral traits in conventional varieties and breeding systems. GCB Bioenergy
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Carter C, Shafir S, Yehonatan L, Palmer RG, Thornburg R (2006) A novel role for proline in plant floral nectars. Naturwissenschaften93: 72-79
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Castro AJ, Clément C (2007) Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study amongthe anther wall, locular fluid and microspore/pollen fractions. Planta 225: 1573-1582
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen L-Q, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of sugars. Annual Review of Biochemistry 84Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J, Kim J-G, Underwood W, Chaudhuri B (2010) Sugartransporters for intercellular exchange and nutrition of pathogens. Nature 468: 527
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen L-Q, Lin IW, Qu X-Q, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressedsucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. The Plant Cell 27: 607-619
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a keystep for phloem transport. Science 335: 207-211
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chiang HH, Dandekar A (1995) Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh during development and inresponse to desiccation. Plant, Cell and Environment 18: 1280-1290
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Clare EL, Schiestl FP, Leitch AR, Chittka L (2013) The promise of genomics in the study of plant-pollinator interactions. GenomeBiology 14: 207
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Clarke A, Considine J, Ward R, Knox R (1977) Mechanism of pollination in Gladiolus: roles of the stigma and pollen-tube guide. Annalsof Botany 41: 15-20
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Collier DE (1997) Changes in respiration, protein and carbohydrates of tulip tepals and Alstroemeria petals during development.Journal of Plant Physiology 150: 446-451
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Coruzzi GM (2003) Primary N-assimilation into amino acids in Arabidopsis. The Arabidopsis Book: e0010Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dancer JE, ap Rees T (1989) Effects of 2, 4-dinitrophenol and anoxia on the inorganic-pyrophosphate content of the spadix of Arummaculatum and the root apices of Pisum sativum. Planta 178: 421-424
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
de Vega C, Herrera CM (2013) Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinatedplant. American Journal of Botany 100: 792-800
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dickinson DB (1965) Germination of lily pollen: respiration and tube growth. Science 150: 1818-1819Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dong Y, Li B, Aharoni A (2016) More than pictures: when MS imaging meets histology. Trends in Plant Science 21: 686-698Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dresselhaus T, Franklin-Tong N (2013) Male–female crosstalk during pollen germination, tube growth and guidance, and doublefertilization. Molecular Plant 6: 1018-1036
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. The Plant Cell 16:S84-S97
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Elleman C, Franklin Tong V, Dickinson H (1992) Pollination in species with dry stigmas: the nature of the early stigmatic response andthe pathway taken by pollen tubes. New Phytologist 121: 413-424
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiology 153: 403-419
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiology138: 2124-2133
CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin I, Qu X-Q, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular andintercellular sugar translocation. Current Opinion in Plant Biology 25: 53-62
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in PlantScience 13: 14-19
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Feng L, Frommer WB (2015) Structure and function of SemiSWEET and SWEET sugar transporters. Trends in Biochemical Sciences40: 480-486
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Feuerstein A, Niedermeier M, Bauer K, Engelmann S, Hoth S, Stadler R, Sauer N (2010) Expression of the AtSUC1 gene in the femalegametophyte, and ecotype specific expression differences in male reproductive organs. Plant Biology 12: 105-114
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Foster J, Lee Y-H, Tegeder M (2008) Distinct expression of members of the LHT amino acid transporter family in flowers indicatesspecific roles in plant reproduction. Sexual Plant Reproduction 21: 143-152
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Franchi GG, Bellani L, Nepi M, Pacini E (1996) Types of carbohydrate reserves in pollen: localization, systematic distribution andecophysiological significance. Flora 191: 143-159
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Franchi GG, Piotto B, Nepi M, Baskin CC, Baskin JM, Pacini E (2011) Pollen and seed desiccation tolerance in relation to degree ofdevelopmental arrest, dispersal, and survival. Journal of experimental botany 62:5267-5281
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environmental Microbiology Reports 4: 97-104Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gahrtz M, Schmelzer E, Stolz J, Sauer N (1996) Expression of the PmSUC1 sucrose carrier gene from Plantago major L. is inducedduring seed development. The Plant Journal 9: 93-100
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gallagher MK, Campbell DR (2017). Shifts in water availability mediate plant–pollinator interactions. New Phytologist 215: 792–802Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gass N, Glagotskaia T, Mellema S, Stuurman J, Barone M, Mandel T, Roessner-Tunali U, Kuhlemeier C (2005) Pyruvate decarboxylaseprovides growing pollen tubes with a competitive advantage in petunia. The Plant Cell 17: 2355-2368
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gaufichon L, Marmagne A, Belcram K, Yoneyama T, Sakakibara Y, Hase T, Grandjean O, Gilles C, Citerne S, Boutet Mercey S (2017)ASN1 encoded asparagine synthetase in floral organs contributes to nitrogen filling in Arabidopsis seeds. The Plant Journal 91: 371–393
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ge YX, Angenent GC, Wittich PE, Peters J, Franken J, Busscher M, Zhang LM, Dahlhaus E, Kater MM, Wullems GJ (2000) NEC1, anovel gene, highly expressed in nectary tissue of Petunia hybrida. The Plant Journal 24: 725-734
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Geigenberger P, Stitt M (1991) A futile cycle of sucrose synthesis and degradation is involved in regulating partitioning betweensucrose, starch and respiration in cotyledons of germinating Ricinus communis L seedlings when phloem transport is inhibited. Planta185: 81-90
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gisel A, Hempel FD, Barella S, Zambryski P (2002) Leaf-to-shoot apex movement of symplastic tracer is restricted coincident withflowering in Arabidopsis. Proceedings of the National Academy of Sciences 99: 1713-1717
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineeringof the carbohydrate supply. Proceedings of the National Academy of Sciences 98: 6522-6527
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Goetz M, Guivarćh A, Hirsche J, Bauerfeind MA, González M-C, Hyun TK, Eom SH, Chriqui D, Engelke T, Großkinsky DK (2017)Metabolic control of tobacco pollination by sugars and invertases. Plant Physiology 173: 984-997
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. The Plant Cell 5: 1217Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57: 761-780Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Guan M, Møller IS, Schjørring JK (2014) Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seedyield structure in Arabidopsis. Journal of Experimental Botany 66: 203-212
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Guan Y-F, Huang X-Y, Zhu J, Gao J-F, Zhang H-X, Yang Z-N (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva genefamily, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiology 147: 852-863
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hafidh S, Fíla J, Honys D (2016) Male gametophyte development and function in angiosperms: a general concept. Plant Reproduction29: 31-51
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in Britishherbaceous plants. Functional Ecology 22: 592-598
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hedhly A, Vogler H, Schmid MW, Pazmino D, Gagliardini V, Santelia D, Grossniklaus U (2016) Starch turnover and metabolism duringflower and early embryo development. Plant Physiology: pp. 00916.02016
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Heil M (2011) Nectar: generation, regulation and ecological functions. Trends in Plant Science 16: 191-200Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Herrera CM, García IM, Pérez R (2008) INVISIBLE FLORAL LARCENIES: MICROBIAL COMMUNITIES DEGRADE FLORAL NECTAR OFBUMBLE BEE POLLINATED PLANTS. Ecology 89: 2369-2376
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hew C, Yip K (1991) Respiration of orchid flower mitochondria. Botanical Gazette 152: 289-295Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Higashiyama T, Yang W-c (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. PlantPhysiology 173: 112-121
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hirsche J, Engelke T, Völler D, Götz M, Roitsch T (2009) Interspecies compatibility of the anther specific cell wall invertase promotersfrom Arabidopsis and tobacco for generating male sterile plants. Theoretical and Applied Genetics 118: 235-245
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ho L, Nichols R (1975) The role of phloem transport in the translocation of sucrose along the stem of carnation cut flowers. Annals ofBotany 39: 439-446
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell'Olivo A, Arnold M, Kuhlemeier C (2007) Single gene–mediatedshift in pollinator attraction in Petunia. The Plant Cell 19: 779-790
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hoekstra F, Crowe L, Crowe J (1989) Differential desiccation sensitivity of corn and Pennisetum pollen linked to their sucrosecontents. Plant, Cell and Environment 12: 83-91
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem andsymplastic unloading of the protein into sink tissues. The Plant Cell 11: 309-322
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ivanov A, Kameka A, Pajak A, Bruneau L, Beyaert R, Hernández-Sebastià C, Marsolais F (2012) Arabidopsis mutants lackingasparaginases develop normally but exhibit enhanced root inhibition by exogenous asparagine. Amino Acids 42: 2307-2318
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jiao J, Mizukami AG, Sankaranarayanan S, Yamguchi J, Itami K, Higashiyama T (2016) Structure-Activity Relation of AMOR SugarMolecule That Activates Pollen-Tubes for Ovular Guidance. Plant Physiology 173: 354-363.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Johnson MA, von Besser K, Zhou Q, Smith E, Aux G, Patton D, Levin JZ, Preuss D (2004) Arabidopsis hapless mutations defineessential gametophytic functions. Genetics 168: 971-982
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter tasting nectar functions as a filter of flower visitors in a bird pollinated plant.Ecology 87: 2709-2716
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jones-Rhoades MW, Borevitz JO, Preuss D (2007) Genome-wide expression profiling of the Arabidopsis female gametophyteidentifies families of small, secreted proteins. PLoS Genetics 3: e171
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Junker RR, Keller A (2015) Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS
Junker RR, Keller A (2015) Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMSMicrobiology Ecology 91: fiv097
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N (2011) Composition of epiphytic bacterial communities differs on petalsand leaves. Plant Biology 13: 918-924
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Junker RR, Romeike T, Keller A, Langen D (2014) Density-dependent negative responses by bumblebees to bacteria isolated fromflowers. Apidologie 45: 467-477
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Karapanos I, Akoumianakis K, Olympios C, Passam HC (2010) Tomato pollen respiration in relation to in vitro germination and pollentube growth under favourable and stress-inducing temperatures. Sexual Plant Reproduction 23: 219-224
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotianaattenuata. The Plant Journal 49: 840-854
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Khan MI, Giridhar P (2015) Plant betalains: chemistry and biochemistry. Phytochemistry 117: 267-295Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kishor PBK, Kumari PH, Sunita M, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and itsimplications in plant ontogeny. Frontiers in Plant Science 6
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E, Guerin PM, Kuhlemeier C (2011) Pollinator choice in Petunia depends ontwo major genetic loci for floral scent production. Current Biology 21: 730-739
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Klepek Y-S, Geiger D, Stadler R, Klebl F, Landouar-Arsivaud L, Lemoine R, Hedrich R, Sauer N (2005) Arabidopsis POLYOLTRANSPORTER5, a new member of the monosaccharide transporter-like superfamily, mediates H+-symport of numerous substrates,including myo-inositol, glycerol, and ribose. The Plant Cell 17: 204-218
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Klepek Y-S, Volke M, Konrad KR, Wippel K, Hoth S, Hedrich R, Sauer N (2009) Arabidopsis thaliana POLYOL/MONOSACCHARIDETRANSPORTERS 1 and 2: fructose and xylitol/H+ symporters in pollen and young xylem cells. Journal of experimental botany 61: 537-550
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Knoch E, Dilokpimol A, Geshi N (2014) Arabinogalactan proteins: focus on carbohydrate active enzymes. Frontiers in Plant Science 5Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Konar R, Linskens H (1966) Physiology and biochemistry of the stigmatic fluid of Petunia hybrida. Planta 71: 372-387Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kram BW, Xu WW, Carter CJ (2009) Uncovering the Arabidopsis thaliana nectary transcriptome: investigation of differential geneexpression in floral nectariferous tissues. BMC Plant Biology 9: 92
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Labarca C, Kroh M, Loewus F (1970) The Composition of Stigmatic Exudate from Lilium longiflorum Labeling Studies with Myo-inositol,d-Glucose, and l-Proline. Plant Physiology 46: 150-156
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Labarca C, Loewus F (1972) The nutritional role of pistil exudate in pollen tube wall formation in Lilium longiflorum I. Utilization ofinjected stigmatic exudate. Plant Physiology 50: 7-14
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink.Annu. Rev. Plant Biol. 55: 341-372
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary cell wall architecture. PlantPhysiology 156: 11-19
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lauxmann MA, Annunziata MG, Brunoud G, Wahl V, Koczut A, Burgos A, Olas JJ, Maximova E, Abel C, Schlereth A (2016) Reproductivefailure in Arabidopsis thaliana under transient carbohydrate limitation: flowers and very young siliques are jettisoned and the meristemis maintained to allow successful resumption of reproductive growth. Plant, Cell and Environment 39: 745-767
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S (2010) Global analysis ofgene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proceedings of theNational Academy of Sciences 107: 8063-8070
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Le Roy K, Vergauwen R, Struyf T, Yuan S, Lammens W, Mátrai J, De Maeyer M, Van den Ende W (2013) Understanding the role ofdefective invertases in plants: tobacco Nin88 fails to degrade sucrose. Plant Physiology 161: 1670-1681
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lee CB, Kim S, McClure B (2009) A pollen protein, NaPCCP, that binds pistil arabinogalactan proteins also binds phosphatidylinositol3-phosphate and associates with the pollen tube endomembrane system. Plant Physiology 149: 791-802
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lee CB, Swatek KN, McClure B (2008) Pollen proteins bind to the C-terminal domain of Nicotiana alata pistil arabinogalactan proteins.Journal of Biological Chemistry 283: 26965-26973
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lenaerts M, Pozo MI, Wäckers F, Van den Ende W, Jacquemyn H, Lievens B (2016) Impact of microbial communities on floral nectarchemistry: potential implications for biological control of pest insects. Basic and Applied Ecology 17: 189-198
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lin IW, Sosso D, Chen L-Q, Gase K, Kim S-G, Kessler D, Klinkenberg PM, Gorder MK, Hou B-H, Qu X-Q (2014) Nectar secretionrequires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508: 546
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Liu G, Ren G, Guirgis A, Thornburg RW (2009) The MYB305 transcription factor regulates expression of nectarin genes in theornamental tobacco floral nectary. The Plant Cell 21: 2672-2687
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology 63:
73-105Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooper BR, Rhodes D, Pichersky E, Dudareva N (2010) RNAi suppression ofArogenate Dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals. ThePlant Cell 22: 832-849
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Maeda H, Yoo H, Dudareva N (2011) Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate. NatureChemical Biology 7: 19-21
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Mascarenhas JP (1970) A new intermediate in plant cell wall synthesis. Biochemical and Biophysical Research Communications 41: 142-149
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Mascarenhas JP (1989) The male gametophyte of flowering plants. The Plant Cell 1: 657Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004) Wounding enhances expression of AtSUC3, a sucrosetransporter from Arabidopsis sieve elements and sink tissues. Plant Physiology 134: 684-693
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Meyer S, Melzer M, Truernit E, HuÈmmer C, Besenbeck R, Stadler R, Sauer N (2000) AtSUC3, a gene encoding a new Arabidopsissucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. The Plant Journal 24: 869-882
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant, Cell and Environment 37: 1936-1949
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Muhlemann JK, Maeda H, Chang C-Y, San Miguel P, Baxter I, Cooper B, Perera MA, Nikolau BJ, Vitek O, Morgan JA (2012)Developmental changes in the metabolic network of snapdragon flowers. PLoS One 7: e40381
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Müller GL, Drincovich MF, Andreo CS, Lara MV (2010) Role of photosynthesis and analysis of key enzymes involved in primarymetabolism throughout the lifespan of the tobacco flower. Journal of Experimental Botany 61: 3675-3688
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182: 31-48Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nepi M (2014) Beyond nectar sweetness: the hidden ecological role of non protein amino acids in nectar. Journal of Ecology 102: 108-115
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nepi M (2017) New perspectives in nectar evolution and ecology: simple alimentary reward or a complex multiorganism interaction?Acta Agrobotanica 70
Nepi M, Franchi G, Padni E (2001) Pollen hydration status at dispersal: cytophysiological features and strategies. Protoplasma 216: 171Pubmed: Author and Title
CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nepi M, Soligo C, Nocentini D, Abate M, Guarnieri M, Cai G, Bini L, Puglia M, Bianchi L, Pacini E (2012) Amino acids and protein profilein floral nectar: much more than a simple reward. Flora-Morphology, Distribution, Functional Ecology of Plants 207: 475-481
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nguyen-Quoc B, Foyer CH (2001). A role for 'futile cycles' involving invertase and sucrose synthase in sucrose metabolism of tomatofruit. Journal of Experimental Botany 52: 881-889.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nicolson SW, Thornburg RW (2007) Nectar chemistry. In Nectaries and nectar. Springer, pp 215-264Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flügge U-I, Schneider A (2005) TheArabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sacdevelopment. The Plant Cell 17: 760-775
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nørholm MH, Nour-Eldin HH, Brodersen P, Mundy J, Halkier BA (2006) Expression of the Arabidopsis high affinity hexose transporterSTP13 correlates with programmed cell death. FEBS Letters 580: 2381-2387
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Noutsos C, Perera AM, Nikolau BJ, Seaver SM, Ware DH (2015) Metabolomic Profiling of the Nectars of Aquilegia pubescens and A.Canadensis. PloS One 10: e0124501
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
O'Neill SD (1997) Pollination regulation of flower development. Annual review of plant biology 48: 547-574Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D (2009) Defensin-likepolypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458: 357-361
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Owen CR, Bradshaw H (2011) Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod-PlantInteractions 5: 235
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pacini E, Franchi G, Hesse M (1985) The tapetum: Its form, function, and possible phylogeny inEmbryophyta. Plant Systematics andEvolution 149: 155-185
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a shortreview. Protoplasma 228: 73-77
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene thatcontrols GABA levels. Cell 114: 47-59
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Persia D, Cai G, Del Casino C, Faleri C, Willemse MT, Cresti M (2008) Sucrose synthase is associated with the cell wall of tobaccopollen tubes. Plant Physiology 147: 1603-1618
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Petanidou T, Van Laere A, N Ellis W, Smets E (2006) What shapes amino acid and sugar composition in Mediterranean floral nectars?Oikos 115: 155-169
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Critical Reviews in Plant Sciences 25: 159-198
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pozo MI, Herrera CM, Lachance MA, Verstrepen K, Lievens B, Jacquemyn H (2016) Species coexistence in simple microbialcommunities: unravelling the phenotypic landscape of co occurring Metschnikowia species in floral nectar. EnvironmentalMicrobiology 18: 1850-1862
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pressman E, Shaked R, Shen S, Altahan L, Firon N (2012) Variations in carbohydrate content and sucrose-metabolizing enzymes intomato (Solanum lycopersicum L.) stamen parts during pollen maturation. Am J Plant Sci 3: 252-260
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Reinders A, Panshyshyn JA, Ward JM (2005) Analysis of transport activity of Arabidopsis sugar alcohol permease homolog AtPLT5.Journal of Biological Chemistry 280: 1594-1602
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBSLetters 581: 2281-2289
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rosen WG, Thomas HR (1970) Secretory cells of lily pistils. I. Fine structure and function. American Journal of Botany: 1108-1114Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rottmann T, Zierer W, Subert C, Sauer N, Stadler R (2016) STP10 encodes a high-affinity monosaccharide transporter and is inducedunder low-glucose conditions in pollen tubes of Arabidopsis. Journal of Experimental Botany 67: 2387-2399
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rounds CM, Winship LJ, Hepler PK (2011) Pollen tube energetics: respiration, fermentation and the race to the ovule. AoB Plants2011: plr019
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Roy R, Schmitt AJ, Thomas JB, Carter CJ (2017) Nectar biology: from molecules to ecosystems. Plant SciencePubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ruan Y-L, Jin Y, Yang Y-J, Li G-J, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development,yield potential, and response to drought and heat. Molecular Plant 3: 942-955
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sassen M (1974) The stylar transmitting tissue. Plant Biology 23: 99-108
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sauer N, Friedländer K, Gräml-Wicke U (1990) Primary structure, genomic organization and heterologous expression of a glucosetransporter from Arabidopsis thaliana. The EMBO Journal 9: 3045
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M, Klebl F (2004) AtSUC8 and AtSUC9 encode functional sucrose transporters, butthe closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. The Plant Journal 40: 120-130
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sauer N, Stolz J (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization inbaker's yeast and identification of the histidine tagged protein. The Plant Journal 6: 67-77
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schaeffer RN, Irwin RE (2014) Yeasts in nectar enhance male fitness in a montane perennial herb. Ecology 95: 1792-1798Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schaeffer RN, Vannette RL, Irwin RE (2015) Nectar yeasts in Delphinium nuttallianum (Ranunculaceae) and their effects on nectarquality. Fungal Ecology 18: 100-106
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schneider S, Hulpke S, Schulz A, Yaron I, Höll J, Imlau A, Schmitt B, Batz S, Wolf S, Hedrich R (2012) Vacuoles release sucrose viatonoplast localised SUC4 type transporters. Plant Biology 14: 325-336
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schneider S, Schneidereit A, Konrad KR, Hajirezaei M-R, Gramann M, Hedrich R, Sauer N (2006) Arabidopsis INOSITOLTRANSPORTER4 mediates high-affinity H+ symport of myoinositol across the plasma membrane. Plant Physiology 141: 565-577
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schneider S, Schneidereit A, Udvardi P, Hammes U, Gramann M, Dietrich P, Sauer N (2007) Arabidopsis INOSITOL TRANSPORTER2mediates H+ symport of different inositol epimers and derivatives across the plasma membrane. Plant Physiology 145: 1395-1407
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schneidereit A, Scholz-Starke J, Büttner M (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9monosaccharide transporter in pollen of Arabidopsis. Plant Physiology 133: 182-190
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schneidereit A, Scholz-Starke J, Sauer N, Büttner M (2005) AtSTP11, a pollen tube-specific monosaccharide transporter inArabidopsis. Planta 221: 48-55
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Scholz-Starke J, Büttner M, Sauer N (2003) AtSTP6, a new pollen-specific H+-monosaccharide symporter from Arabidopsis. PlantPhysiology 131: 70-77
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline,glycine betaine, and γ-amino butyric acid in tomato pollen. The Plant Cell 11: 377-391
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sedio BE (2017) Recent breakthroughs in metabolomics promise to reveal the cryptic chemical traits that mediate plant communitycomposition, character evolution and lineage diversification. New Phytologist 214: 952-958
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Seymour RS (1999) Pattern of respiration by intact inflorescences of the thermogenic arum lily Philodendron selloum. Journal ofExperimental Botany 50: 845-852
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sheehan H, Moser M, Klahre U, Esfeld K, Dell'Olivo A, Mandel T, Metzger S, Vandenbussche M, Freitas L, Kuhlemeier C (2016) MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation. Naturegenetics 48: 159
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Singh MB, Knox RB (1984) Invertases of Lilium pollen Characterization and activity during in vitro germination. Plant Physiology 74:510-515
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sivitz AB, Reinders A, Ward JM (2008) Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiology 147: 92-100
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sklensky DE, Davies PJ (2011) Resource partitioning to male and female flowers of Spinacia oleracea L. in relation to whole-plantmonocarpic senescence. Journal of Experimental Botany 62: 4323-4336
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell and Environment 30: 1126-1149Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sosso D, Luo D, Li Q-B, Sasse J, Yang J, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS (2015) Seed filling in domesticatedmaize and rice depends on SWEET-mediated hexose transport. Nature Genetics 47: 1489
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outerintegument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiology 139: 701-712
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for antherdehiscence and pollen tube growth in Arabidopsis. The Plant Journal 19: 269-278
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sun M-X, Huang X-Y, Yang J, Guan Y-F, Yang Z-N (2013) Arabidopsis RPG1 is important for primexine deposition and functionsredundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reproduction 26: 83-91
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants inArabidopsis. PLoS Biology 10: e1001449
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal 54:733-749
CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tegeder M (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Current Opinion in Plant Biology 15:315-321
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tegeder M, Rentsch D (2010) Uptake and partitioning of amino acids and peptides. Molecular Plant 3: 997-1011Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. Journal of Experimental Botany 54: 1127-1132Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Truernit E, Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196: 564-570
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhancedexpression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. The Plant Cell 8: 2169-2182
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Truernit E, Stadler R, Baier K, Sauer N (1999) A male gametophyte specific monosaccharide transporter inArabidopsis. The PlantJournal 17: 191-201
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tsanakas GF, Manioudaki ME, Economou AS, Kalaitzis P (2014) De novo transcriptome analysis of petal senescence in Gardeniajasminoides Ellis. BMC Genomics 15: 554
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
van Doorn WG, Kamdee C (2014) Flower opening and closure: an update. Journal of Experimental Botany 65: 5749-5757Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
van Doorn WG, van Meeteren U (2003) Flower opening and closure: a review. Journal of Experimental Botany 54: 1801-1812Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014) How does pollen chemistry impactdevelopment and feeding behaviour of polylectic bees? PLoS One 9: e86209
Vanderplanck M, Vereecken NJ, Grumiau L, Esposito F, Lognay G, Wattiez R, Michez D (2017) The importance of pollen chemistry inevolutionary host shifts of bees. Scientific Reports 7
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Vannette RL, Fukami T (2016) Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption bypollinators. Ecology 97: 1410-1419
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Vannette RL, Gauthier M-PL, Fukami T (2013) Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proceedings of theRoyal Society of London B: Biological Sciences 280: 20122601
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wagstaff C, Yang TJ, Stead AD, Buchanan Wollaston V, Roberts JA (2009) A molecular and structural characterization of senescing
Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. The Plant Journal 57: 690-705Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wang L, Ruan Y-L (2016) Critical roles of vacuolar invertase in floral organ development and male and female fertilities are revealedthrough characterization of GhVIN1-RNAi cotton plants. Plant Physiology 171: 405-423
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Weber H, Borisjuk L, Wobus U (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2: 169-174Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Weiner CN, Hilpert A, Werner M, Linsenmair KE, Blüthgen N (2010) Pollen amino acids and flower specialisation in solitary bees.Apidologie 41: 476-487
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB, Ward JM (2000) A new subfamily of sucrose transporters, SUT4,with low affinity/high capacity localized in enucleate sieve elements of plants. The Plant Cell 12: 1345-1355
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Weiss D, Schönfeld M, Halevy AH (1988) Photosynthetic activities in the Petunia corolla. Plant Physiology 87: 666-670Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Werner D, Gerlitz N, Stadler R (2011) A dual switch in phloem unloading during ovule development in Arabidopsis. Protoplasma 248:225-235
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Widhalm JR, Gutensohn M, Yoo H, Adebesin F, Qian Y, Guo L, Jaini R, Lynch JH, McCoy RM, Shreve JT (2015) Identification of aplastidial phenylalanine exporter that influences flux distribution through the phenylalanine biosynthetic network. NatureCommunications 6
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wiesen LB, Bender RL, Paradis T, Larson A, Perera MAD, Nikolau BJ, Olszewski NE, Carter CJ (2016) A Role for GIBBERELLIN 2-OXIDASE6 and Gibberellins in Regulating Nectar Production. Molecular Plant 9: 753-756
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ylstra B, Garrido D, Busscher J, van Tunen AJ (1998) Hexose transport in growing petunia pollen tubes and characterization of apollen-specific, putative monosaccharide transporter. Plant Physiology 118: 297-304
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yoo H, Widhalm JR, Qian Y, Maeda H, Cooper BR, Jannasch AS, Gonda I, Lewinsohn E, Rhodes D, Dudareva N (2013) An alternativepathway contributes to phenylalanine biosynthesis in plants via a cytosolic tyrosine: phenylpyruvate aminotransferase. NatureCommunications 4: 2833
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yuan Y-W, Byers KJ, Bradshaw H (2013) The genetic control of flower–pollinator specificity. Current opinion in plant biology 16: 422-428
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhou Y, Li M, Zhao F, Zha H, Yang L, Lu Y, Wang G, Shi J, Chen J (2016) Floral Nectary Morphology and Proteomic Analysis of Nectar ofLiriodendron tulipifera Linn. Frontiers in Plant Science 7
Pubmed: Author and TitleCrossRef: Author and Title