Dynamics of Candidatus Liberibacter asiaticus Movement and ...€¦ · 09/12/2019 · 2 26 27 28 Abstract 29 Citrus greening or Huanglongbing (HLB) is caused by the phloem-limited
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1
Short title: Candidatus Liberibacter asiaticus Phloem Movement 1
Corresponding author: Amit Levy 2
3
Dynamics of Candidatus Liberibacter asiaticus Movement and Sieve-Pore 4
Plugging in Citrus Sink Cells 5
Diann Achor1, Stacy Welker 1,2 , Sulley Ben-Mahmoud 1,*, Chunxia Wang 1 , Svetlana Y. Folimonova2, 6
Manjul Dutt 1,3, Siddarame Gowda1,2, and Amit Levy1,2 7
1Citrus research and Education Center, University of Florida, Lake Alfred, FL 8
2Department of Plant Pathology, University of Florida, Gainesville, FL 9
3Horticultural Sciences Department, University of Florida, Gainesville, FL 10
11
One-sentence summary: The phloem-limited Gram-negative bacterium Candidatus Liberibacter 12
asiaticus interacts with the phloem membranes of citrus species and can change its form to move 13
through the phloem pores. 14
15
List of author contributions: A.L., S.Y.F., D.A., M.D., and S.G. designed the experiments, D.A., S.W., C.W., 16
and S.B-M. collected the data, A.L., S.W., and S.B-M. analyzed the data, A.L. conceived the project and 17
wrote the article with contributions of all the authors. 18
19
Funding information: The work was supported by UF/IFAS early career seed grant (No. 00127818) to 20
A.L. 21
22
Present address: *Department of Entomology, University of California, Davis, CA (S.B-M.) 23
TEM cross-section micrographs of HLB-infected Duncan grapefruit (A, B and F) and sweet orange (C-E) 478
seed coats (A-B), flush (C-D), and roots (E-F). (A-C) Attachment of CLas bacteria to the host cell 479
membrane adjacent to the phloem pores through an unknown filamentous material (black arrows). (D-480
F) Attachment of CLas bacteria to the host cell membrane adjacent to the phloem pores through an 481
anchor-like link (black arrows). 482
483
484
References: 485
486
Achor DS, Etxeberria E, Wang N, Folimonova SY, Chung KR, Albrigo LB (2010) Sequence of Anatomical 487 Symptom Observations in Citrus Affected with Huanglongbing Disease. Plant Pathology Journal 488 9: 56-64. 489
490 Aloni R, Raviv A, Peterson CA (1991) The Role of Auxin in the Removal of Dormancy Callose and 491
Resumption of Phloem Activity in Vitis-Vinifera. Canadian Journal of Botany-Revue Canadienne 492 De Botanique 69: 1825-1832 493
Aritua V, Achor D, Gmitter FG, Albrigo G, Wang N (2013) Transcriptional and Microscopic Analyses of 494 Citrus Stem and Root Responses to Candidatus Liberibacter asiaticus Infection. PLOS ONE 8: 495 e73742 496
Barratt DHP, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose 497 Synthase GSL7 Is Necessary for Normal Phloem Transport and Inflorescence Growth in 498 Arabidopsis. Plant Physiology 155: 328-341 499
Behnke HD, Sjolund RD (1990) Sieve Elements. Springer-Verlag, Berlin Heidelberg New York 500 Bove JM (2006) Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of 501
Plant Pathology 88: 7-37 502 Buxa SV, Degola F, Polizzotto R, De Marco F, Loschi A, Kogel K-H, di Toppi LS, van Bel AJE, Musetti R 503
(2015) Phytoplasma infection in tomato is associated with re-organization of plasma membrane, 504 ER stacks, and actin filaments in sieve elements. Frontiers in Plant Science 6 505
Cui W, Lee J-Y (2016) Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during 506 stress. Nature Plants 2: 16034 507
De Storme N, Geelen D (2014) Callose homeostasis at plasmodesmata: molecular regulators and 508 developmental relevance. Frontiers in Plant Science 5 509
Deng H, Achor D, Exteberria E, Yu Q, Du D, Stanton D, Liang G, Gmitter Jr. FG (2019) Phloem 510 Regeneration Is a Mechanism for Huanglongbing-Tolerance of “Bearss” Lemon and “LB8-9” 511 Sugar Belle® Mandarin. Frontiers in Plant Science 10 512
Etxeberria E, Gonzalez P, Achor D, Albrigo G (2009) Anatomical distribution of abnormally high levels of 513 starch in HLB-affected Valencia orange trees. Physiological and Molecular Plant Pathology 74: 514 76-83 515
Folimonova SY, Achor DS (2010) Early Events of Citrus Greening (Huanglongbing) Disease Development 516 at the Ultrastructural Level. Phytopathology 100: 949-958 517
Furch ACU, Hafke JB, van Bel AJE, Schulz A (2007) Ca2+-mediated remote control of reversible sieve 518 tube occlusion in Vicia faba. Journal of Experimental Botany 58: 2827-2838 519
Granato LM, Galdeano DM, D’Alessandre NDR, Breton MC, Machado MA (2019) Callose synthase 520 family genes plays an important role in the Citrus defense response to Candidatus Liberibacter 521 asiaticus. European Journal of Plant Pathology 155: 25-38 522
Harper SJ, Cowell SJ, Robertson CJ, Dawson WO (2014) Differential tropism in roots and shoots infected 523 by Citrus tristeza virus. Virology 460-461: 91-99 524
Hartung JS, Halbert SE, Pelz-Stelinski K, Brlansky RH, Chen C, Gmitter FG (2010) Lack of Evidence for 525 Transmission of ‘Candidatus Liberibacter asiaticus’ Through Citrus Seed Taken from Affected 526 Fruit. Plant Disease 94: 1200-1205 527
Hilf ME, Sims KR, Folimonova SY, Achor DS (2013) Visualization of ‘Candidatus Liberibacter asiaticus’ 528 Cells in the Vascular Bundle of Citrus Seed Coats with Fluorescence In Situ Hybridization and 529 Transmission Electron Microscopy. Phytopathology 103: 545-554 530
Hollis CA, Tepper HB (1971) Auxin Transport within Intact Dormant and Active White Ash Shoots. Plant 531 Physiology 48: 146-149 532
Johnson EG, Wu J, Bright DB, Graham JH (2014) Association of ‘Candidatus Liberibacter asiaticus’ root 533 infection, but not phloem plugging with root loss on huanglongbing-affected trees prior to 534 appearance of foliar symptoms. Plant Pathology 63: 290-298 535
Kim J-S, Sagaram US, Burns JK, Li J-L, Wang N (2008) Response of Sweet Orange (Citrus sinensis) to 536 ˜Candidatus Liberibacter asiaticus" Infection: Microscopy and Microarray Analyses. 537 Phytopathology 99: 50-57 538
Knoblauch M, Froelich DR, Pickard WF, Peters WS (2014) SEORious business: structural proteins in sieve 539 tubes and their involvement in sieve element occlusion. Journal of Experimental Botany 65: 540 1879-1893 541
Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible Calcium-Regulated Stopcocks in 542 Legume Sieve Tubes. The Plant Cell 13: 1221-1230 543
Knoblauch M, van Bel AJE (1998) Sieve Tubes in Action. The Plant Cell 10: 35-50 544 Koh E-J, Zhou L, Williams DS, Park J, Ding N, Duan Y-P, Kang B-H (2012) Callose deposition in the 545
phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with 546 "Candidatus Liberibacter asiaticus". Protoplasma 249: 687-697 547
Levy A, Zheng JY, Lazarowitz SG (2015) Synaptotagmin SYTA Forms ER-Plasma Membrane Junctions that 548 Are Recruited to Plasmodesmata for Plant Virus Movement. Current Biology 25: 2018-2025 549
Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative 550 PCR and the 2−ΔΔCT Method. Methods 25: 402-408 551
Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low-temperature 552 adaptation and phloem loading in Arabidopsis. Plant Cell 18: 2710-2732 553
McNairn RB (1972) Phloem Translocation and Heat-Induced Callose Formation in Field-Grown 554 Gossypium-Hirsutum-L. Plant Physiology 50: 366-& 555
McNairn RB, Currier HB (1968) Translocation Blockage by Sieve Plate Callose. Planta 82: 369-& 556 Musetti R, Pagliari L, Buxa SV, Degola F, De Marco F, Loschi A, Kogel K-H, van Bel AJE (2016) OHMS**: 557
Phytoplasmas dictate changes in sieve-element ultrastructure to accommodate their 558 requirements for nutrition, multiplication and translocation AU - Musetti, Rita. Plant Signaling & 559 Behavior 11: e1138191 560
Raffaele S, Bayer E, Lafarge D, Cluzet S, Retana SG, Boubekeur T, Leborgne-Castel N, Carde JP, 561 Lherminier J, Noirot E, Satiat-Jeunemaitre B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, 562 Reymond P, Simon-Plas F, Farmer EE, Bessoule JJ, Mongrand S (2009) Remorin, a Solanaceae 563 Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement. 564 Plant Cell 21: 1541-1555 565
Read SM, Northcote DH (1983) Chemical and Immunological Similarities between the Phloem Proteins 566 of 3 Genera of the Cucurbitaceae. Planta 158: 119-127 567
Siller W, Kuhbandner B, Marwitz R, Petzold H, Seemüller E (1987) Occurrence of Mycoplasma-like 568 Organisms in Parenchyma Cells of Cuscuta odorata (Ruiz et Pav.). Journal of Phytopathology 569 119: 147-159 570
Stone BA, Clarke AE (1992) Chemistry and Physiology of Higher Plants (1->3)-beta-glucans. In BA Stone, 571 AE Clarke, eds, Chemistry and Biology of (1->3)-beta-glucans. La Trobe University Press, Victoria 572 Australia, pp 365-429 573
Tatineni S, Sagaram US, Gowda S, Robertson CJ, Dawson WO, Iwanami T, Wang N (2008) In Planta 574 Distribution of ‘Candidatus Liberibacter asiaticus’ as Revealed by Polymerase Chain Reaction 575 (PCR) and Real-Time PCR. Phytopathology 98: 592-599 576
Voigt CA, Ellinger D (2014) Callose biosynthesis in arabidopsis with a focus on pathogen response: what 577 we have learned within the last decade. Annals of Botany 114: 1349-1358 578
Wang Y, Zhou L, Yu X, Stover E, Luo F, Duan Y (2016) Transcriptome Profiling of Huanglongbing (HLB) 579 Tolerant and Susceptible Citrus Plants Reveals the Role of Basal Resistance in HLB Tolerance. 580 Frontiers in Plant Science 7 581
Webster DB, Currier HH (1965) Callose - Lateral Movement of Assimilates from Phloem. Science 150: 582 1610-& 583
Xie B, Hong Z (2011) Unplugging the callose plug from sieve pores. Plant Signaling & Behavior 6: 491-493 584 Xie B, Wang X, Zhu M, Zhang Z, Hong Z (2010) CalS7 encodes a callose synthase responsible for callose 585
deposition in the phloem. The Plant Journal 65: 1-14 586 Yusa A, Maejima K, Himeno M, Netsu O, Namba S, Nijo T, Tomomitsu T, Neriya Y, Hamamoto H, 587
Oshima K (2014) Onion yellow phytoplasma P38 protein plays a role in adhesion to the hosts. 588 FEMS Microbiology Letters 361: 115-122 589
Zavaliev R, Ueki S, Epel BL, Citovsky V (2011) Biology of callose (beta-1,3-glucan) turnover at 590 plasmodesmata. Protoplasma 248: 117-130 591
Zhong Y, Cheng C-z, Jiang N-h, Jiang B, Zhang Y-y, Wu B, Hu M-l, Zeng J-w, Yan H-x, Yi G-j, Zhong G-y 592 (2015) Comparative Transcriptome and iTRAQ Proteome Analyses of Citrus Root Responses to 593 Candidatus Liberibacter asiaticus Infection. PLOS ONE 10: e0126973 594
Parsed CitationsAchor DS, Etxeberria E, Wang N, Folimonova SY, Chung KR, Albrigo LB (2010) Sequence of Anatomical Symptom Observations inCitrus Affected with Huanglongbing Disease. Plant Pathology Journal 9: 56-64.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Aloni R, Raviv A, Peterson CA (1991) The Role of Auxin in the Removal of Dormancy Callose and Resumption of Phloem Activity inVitis-Vinifera. Canadian Journal of Botany-Revue Canadienne De Botanique 69: 1825-1832
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Aritua V, Achor D, Gmitter FG, Albrigo G, Wang N (2013) Transcriptional and Microscopic Analyses of Citrus Stem and Root Responsesto Candidatus Liberibacter asiaticus Infection. PLOS ONE 8: e73742
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Barratt DHP, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose Synthase GSL7 Is Necessary forNormal Phloem Transport and Inflorescence Growth in Arabidopsis. Plant Physiology 155: 328-341
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Behnke HD, Sjolund RD (1990) Sieve Elements. Springer-Verlag, Berlin Heidelberg New YorkPubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bove JM (2006) Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88: 7-37Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Buxa SV, Degola F, Polizzotto R, De Marco F, Loschi A, Kogel K-H, di Toppi LS, van Bel AJE, Musetti R (2015) Phytoplasma infection intomato is associated with re-organization of plasma membrane, ER stacks, and actin filaments in sieve elements. Frontiers in PlantScience 6
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Cui W, Lee J-Y (2016) Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nature Plants 2: 16034Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
De Storme N, Geelen D (2014) Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Frontiersin Plant Science 5
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Deng H, Achor D, Exteberria E, Yu Q, Du D, Stanton D, Liang G, Gmitter Jr. FG (2019) Phloem Regeneration Is a Mechanism forHuanglongbing-Tolerance of "Bearss" Lemon and "LB8-9" Sugar Belle® Mandarin. Frontiers in Plant Science 10
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Etxeberria E, Gonzalez P, Achor D, Albrigo G (2009) Anatomical distribution of abnormally high levels of starch in HLB-affectedValencia orange trees. Physiological and Molecular Plant Pathology 74: 76-83
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Folimonova SY, Achor DS (2010) Early Events of Citrus Greening (Huanglongbing) Disease Development at the Ultrastructural Level.Phytopathology 100: 949-958
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Furch ACU, Hafke JB, van Bel AJE, Schulz A (2007) Ca2+-mediated remote control of reversible sieve tube occlusion in Vicia faba.Journal of Experimental Botany 58: 2827-2838
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Granato LM, Galdeano DM, D'Alessandre NDR, Breton MC, Machado MA (2019) Callose synthase family genes plays an important rolein the Citrus defense response to Candidatus Liberibacter asiaticus. European Journal of Plant Pathology 155: 25-38
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Harper SJ, Cowell SJ, Robertson CJ, Dawson WO (2014) Differential tropism in roots and shoots infected by Citrus tristeza virus.Virology 460-461: 91-99
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon September 18, 2020 - Published by Downloaded from
Hartung JS, Halbert SE, Pelz-Stelinski K, Brlansky RH, Chen C, Gmitter FG (2010) Lack of Evidence for Transmission of 'CandidatusLiberibacter asiaticus' Through Citrus Seed Taken from Affected Fruit. Plant Disease 94: 1200-1205
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hilf ME, Sims KR, Folimonova SY, Achor DS (2013) Visualization of 'Candidatus Liberibacter asiaticus' Cells in the Vascular Bundle ofCitrus Seed Coats with Fluorescence In Situ Hybridization and Transmission Electron Microscopy. Phytopathology 103: 545-554
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hollis CA, Tepper HB (1971) Auxin Transport within Intact Dormant and Active White Ash Shoots. Plant Physiology 48: 146-149Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Johnson EG, Wu J, Bright DB, Graham JH (2014) Association of 'Candidatus Liberibacter asiaticus' root infection, but not phloemplugging with root loss on huanglongbing-affected trees prior to appearance of foliar symptoms. Plant Pathology 63: 290-298
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kim J-S, Sagaram US, Burns JK, Li J-L, Wang N (2008) Response of Sweet Orange (Citrus sinensis) to ˜Candidatus Liberibacterasiaticus" Infection: Microscopy and Microarray Analyses. Phytopathology 99: 50-57
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Knoblauch M, Froelich DR, Pickard WF, Peters WS (2014) SEORious business: structural proteins in sieve tubes and their involvementin sieve element occlusion. Journal of Experimental Botany 65: 1879-1893
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible Calcium-Regulated Stopcocks in Legume Sieve Tubes. The PlantCell 13: 1221-1230
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Knoblauch M, van Bel AJE (1998) Sieve Tubes in Action. The Plant Cell 10: 35-50Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Koh E-J, Zhou L, Williams DS, Park J, Ding N, Duan Y-P, Kang B-H (2012) Callose deposition in the phloem plasmodesmata andinhibition of phloem transport in citrus leaves infected with "Candidatus Liberibacter asiaticus". Protoplasma 249: 687-697
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Levy A, Zheng JY, Lazarowitz SG (2015) Synaptotagmin SYTA Forms ER-Plasma Membrane Junctions that Are Recruited toPlasmodesmata for Plant Virus Movement. Current Biology 25: 2018-2025
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCTMethod. Methods 25: 402-408
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low-temperature adaptation and phloem loading inArabidopsis. Plant Cell 18: 2710-2732
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
McNairn RB (1972) Phloem Translocation and Heat-Induced Callose Formation in Field-Grown Gossypium-Hirsutum-L. Plant Physiology50: 366-&
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
McNairn RB, Currier HB (1968) Translocation Blockage by Sieve Plate Callose. Planta 82: 369-&Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Musetti R, Pagliari L, Buxa SV, Degola F, De Marco F, Loschi A, Kogel K-H, van Bel AJE (2016) OHMS**: Phytoplasmas dictate changesin sieve-element ultrastructure to accommodate their requirements for nutrition, multiplication and translocation AU - Musetti, Rita.Plant Signaling & Behavior 11: e1138191
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jeunemaitre B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule JJ, Mongrand S (2009)Remorin, a Solanaceae Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement. Plant Cell 21:1541-1555
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Read SM, Northcote DH (1983) Chemical and Immunological Similarities between the Phloem Proteins of 3 Genera of theCucurbitaceae. Planta 158: 119-127
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Siller W, Kuhbandner B, Marwitz R, Petzold H, Seemüller E (1987) Occurrence of Mycoplasma-like Organisms in Parenchyma Cells ofCuscuta odorata (Ruiz et Pav.). Journal of Phytopathology 119: 147-159
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stone BA, Clarke AE (1992) Chemistry and Physiology of Higher Plants (1->3)-beta-glucans. In BA Stone, AE Clarke, eds, Chemistry andBiology of (1->3)-beta-glucans. La Trobe University Press, Victoria Australia, pp 365-429
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tatineni S, Sagaram US, Gowda S, Robertson CJ, Dawson WO, Iwanami T, Wang N (2008) In Planta Distribution of 'CandidatusLiberibacter asiaticus' as Revealed by Polymerase Chain Reaction (PCR) and Real-Time PCR. Phytopathology 98: 592-599
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Voigt CA, Ellinger D (2014) Callose biosynthesis in arabidopsis with a focus on pathogen response: what we have learned within thelast decade. Annals of Botany 114: 1349-1358
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wang Y, Zhou L, Yu X, Stover E, Luo F, Duan Y (2016) Transcriptome Profiling of Huanglongbing (HLB) Tolerant and Susceptible CitrusPlants Reveals the Role of Basal Resistance in HLB Tolerance. Frontiers in Plant Science 7
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Webster DB, Currier HH (1965) Callose - Lateral Movement of Assimilates from Phloem. Science 150: 1610-&Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Xie B, Hong Z (2011) Unplugging the callose plug from sieve pores. Plant Signaling & Behavior 6: 491-493Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Xie B, Wang X, Zhu M, Zhang Z, Hong Z (2010) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. ThePlant Journal 65: 1-14
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yusa A, Maejima K, Himeno M, Netsu O, Namba S, Nijo T, Tomomitsu T, Neriya Y, Hamamoto H, Oshima K (2014) Onion yellowphytoplasma P38 protein plays a role in adhesion to the hosts. FEMS Microbiology Letters 361: 115-122
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zavaliev R, Ueki S, Epel BL, Citovsky V (2011) Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma 248: 117-130
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhong Y, Cheng C-z, Jiang N-h, Jiang B, Zhang Y-y, Wu B, Hu M-l, Zeng J-w, Yan H-x, Yi G-j, Zhong G-y (2015) ComparativeTranscriptome and iTRAQ Proteome Analyses of Citrus Root Responses to Candidatus Liberibacter asiaticus Infection. PLOS ONE 10:e0126973
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title