1 Author for contact: Claus-Peter Witte 1 , Leibniz Universität Hannover, Department of 1 Molecular Nutrition and Biochemistry of Plants, Herrenhäuser Str. 2, 30419 Hannover, 2 Germany 3 Update: Nucleotide Metabolism in Plants 4 Claus-Peter Witte a,2,3 and Marco Herde a 5 a Leibniz Universität Hannover, Department of Molecular Nutrition and Biochemistry of 6 Plants, Herrenhäuser Str. 2, 30419 Hannover, Germany 7 2 Author for contact 8 3 Senior author 9 ORCID ID: 0000-0002-3617-7807 (C.-P.W.) 10 ORCID ID: 0000-0003-2804-0613 (M.H.) 11 One-sentence summary: Nucleotide metabolism is an essential function in plants. 12 13 Author contributions: C.-P.W. conceived the study, C.-P.W. and M.H. wrote the article 14 Funding: The authors acknowledge funding from the Deutsche Forschungsgemeinschaft 15 (WI3411/4-1 to C.-P.W. and HE 5949/3-1 to M.H.) and the Bundesministerium für Bildung 16 und Forschung (Nutzpflanzen der Zukunft - 031B0540). 17 E-mail address of the author for contact: [email protected]18 19 Nucleotide metabolism in plants 20 Nucleotides are essential for life. It is easy to validate this statement – one just needs to 21 recall that nucleotides are the building blocks of DNA and RNA, and that many molecules 22 which are central for metabolism, for example ATP, NADH, Co-A and UDP-glucose, are 23 nucleotides or contain nucleotide moieties. Generally, a nucleotide is defined as a 24 phosphorylated ribose or deoxyribose linked to a nitrogen-containing heterocyclic group 25 called the nucleobase via a glycosidic bond (Figure 1). Because of the phosphate groups, 26 nucleotides are negatively charged, whereas at neutral pH nucleosides and nucleobases are 27 uncharged. The exception is xanthine, which is partially charged as a free base (pKa = 7.4) 28 but completely charged at the base in xanthosine (pKa = 5.5) or the corresponding 29 nucleotides (Figure 1, Sigel et al., 2009). 30 Many excellent reviews focus on general (Wagner and Backer, 1992; Zrenner et al., 2006; 31 Zrenner and Ashihara, 2011; Stasolla et al., 2003; Moffatt and Ashihara, 2002) or particular 32 Plant Physiology Preview. Published on October 22, 2019, as DOI:10.1104/pp.19.00955 Copyright 2019 by the American Society of Plant Biologists https://plantphysiol.org Downloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
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1
Author for contact: Claus-Peter Witte 1, Leibniz Universität Hannover, Department of 1
Molecular Nutrition and Biochemistry of Plants, Herrenhäuser Str. 2, 30419 Hannover, 2
Germany 3
Update: Nucleotide Metabolism in Plants 4
Claus-Peter Wittea,2,3 and Marco Herdea 5
a Leibniz Universität Hannover, Department of Molecular Nutrition and Biochemistry of 6
Plants, Herrenhäuser Str. 2, 30419 Hannover, Germany 7
2 Author for contact 8 3 Senior author 9
ORCID ID: 0000-0002-3617-7807 (C.-P.W.) 10
ORCID ID: 0000-0003-2804-0613 (M.H.) 11
One-sentence summary: Nucleotide metabolism is an essential function in plants. 12
13
Author contributions: C.-P.W. conceived the study, C.-P.W. and M.H. wrote the article 14
Funding: The authors acknowledge funding from the Deutsche Forschungsgemeinschaft 15
(WI3411/4-1 to C.-P.W. and HE 5949/3-1 to M.H.) and the Bundesministerium für Bildung 16
und Forschung (Nutzpflanzen der Zukunft - 031B0540). 17
aspects of (Smith and Atkins, 2002; Ashihara et al., 2018; Kafer et al., 2004) plant nucleotide 33
metabolism. The aim of this review is to provide an update on how nucleotide metabolism is 34
hardwired, mostly focusing on the cellular level, because our understanding of the 35
organization at the tissue and organ level remains very limited. The presented models are 36
mostly based on results from Arabidopsis thaliana. These will often be valid for most plants, 37
but certainly there will be species-dependent variations. We also cover extracellular 38
nucleotide metabolism and review the evidence for overlap between cytokinin metabolism 39
and central nucleotide metabolism. Figure 2 shows a general overview of plant nucleotide 40
metabolism. 41
DE NOVO SYNTHESIS 42
Purine de novo synthesis 43
Plants possess the metabolic pathways for the de novo synthesis of purine nucleotides 44
generating AMP as well as pyrimidine nucleotides yielding UMP. During de novo 45
biosynthesis, nucleotides are newly synthesized from the general metabolites activated 46
ribose (5-phosphoribosyl-1-pyrophosphate, PRPP), glutamine, aspartate, and bicarbonate as 47
well as specifically for the purine nucleotides, glycine and formyl tetrahydrofolate (Figure 2). 48
There is strong evidence that AMP biosynthesis occurs entirely in the plastids, because the 49
11 enzymes (catalyzing 12 reactions; Smith and Atkins, 2002) required for AMP biosynthesis 50
in Arabidopsis all have an N-terminal organelle targeting peptide, and C-terminal yellow 51
fluorescent protein (YFP)-fusion proteins of several of these enzymes were observed 52
exclusively in the plastids when they were transiently expressed in Nicotiana benthamiana 53
in our laboratory (N. Medina Escobar and C.-P. Witte, unpublished data) (Figure 3A). In rice 54
(Oryza sativa), the pathway also seems to reside in plastids (Zhang et al., 2018). However, it 55
has been reported that in nodules of the tropical legume cowpea (Vigna unguiculata), 56
purine biosynthesis is targeted to plastids and mitochondria (Atkins et al., 1997; Smith and 57
Atkins, 2002). It may be worthwhile to reconfirm this special localization in nodules using 58
fluorescent tagged proteins. 59
AMP is exported from the plastids by the adenine nucleotide uniporter brittle1 (BT1, Figure 60
3A, number 1), which can also transport ADP and ATP (Hu et al., 2017; Kirchberger et al., 61
2008; Leroch et al., 2005). Interestingly, BT1 from Arabidopsis and maize (Zea mays) was 62
reported to be dual localized to the chloroplast and mitochondria (Bahaji et al., 2011b) and 63 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
The final steps of UMP, GMP and CTP biosynthesis occur in the cytosol. With the exception 126
of CTP, which is directly synthesized from UTP, purine and pyrimidine nucleoside 127
triphosphate synthesis is achieved by phosphorylation of the respective monophosphates 128
(Figure 4). 129
The plastids and the mitochondria, which possess their own transcription and translation 130
machineries, must be supplied with ribonucleotides and deoxyribonucleotides from the 131
cytosol. Not much is known about (i) the phosphorylation state in which nucleotides are 132
taken up, (ii) which transporters are involved, (iii) if the concentrations of (desoxy) 133
nucleotides differ in the distinct cellular compartments and how this may be regulated –134
subcellular distributions have been estimated only for the adenylates (Stitt et al., 1982). 135
Describing the subcellular distribution of the enzymes involved in the last two steps of 136
mononucleotide phosphorylation can help in building hypotheses regarding the exact 137
nucleotide species imported into organelles. 138
The pyrimidine nucleotides, UMP and CMP, are phosphorylated by UMP kinases (UMK, 139
Figure 4, A and B, #12) Arabidopsis possess two evolutionarily distinct families of such 140
enzymes (i) UMKs related to adenylate kinases (AMKs) encoded by four genes and (ii) UMKs 141
related to eubacterial UMP kinases encoded by two genes. The AMK-like UMKs have not yet 142
been characterized, except for a biochemical analysis of UMK3 (At5g26667), which was 143
shown to utilize UMP and CMP as the best substrates (Zhou et al., 1998). These enzymes 144
have been predicted to reside in the cytosol and the mitochondria (Lange et al., 2008). From 145
the eubacterial UMP kinase family, one member called ‘plastid UMP kinase’ (PUMKIN, 146
At3g18680) was shown to be located in chloroplasts, and to have UMK activity in vitro. 147
Interestingly, the enzyme binds certain plastidic transcripts and is involved in plastid RNA 148
metabolism, which may not require its enzymatic function. Mutants are small and 149
compromised in plastid translation and photosynthetic performance (Schmid et al., 2019). 150
The orthologous enzyme in rice is localized in chloroplasts, participates in RNA metabolism, 151
and the corresponding loss-of-function mutants are pale green (Chen et al., 2018a; Zhu et 152
al., 2016). Additionally, they contain less UDP and more UMP (Dong et al., 2019) suggesting 153
that UMP phosphorylation in the chloroplast is functionally important. The phosphorylation 154
of TMP is not catalyzed by UMKs, but by a dedicated thymidine monophosphate kinase 155 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
prevents the formation of N6-methyl ATP, which is a substrate of RNA polymerase II (Chen 186
et al., 2018b). 187
Recently, a broad spectrum mononucleotide kinase only distantly related to the AMKs, but 188
with relatively high adenylate kinase activity was described (At5g60340). This enzyme was 189
localized in the nucleus and a knockout mutant was affected in stem elongation (Feng et al., 190
2012). 191
Plastids and mitochondria possess nucleoside monophosphate kinases for all nucleotides. 192
Thus, nucleoside monophosphates are probably imported into these organelles and are 193
phosphorylated to dinucleotides. Enzymes catalyzing the next step to trinucleotides, the 194
nucleoside diphosphate kinases (NDPKs), should therefore be found in plastids and 195
mitochondria as well as in the cytosol. This has been indeed observed (Luzarowski et al., 196
2017). The exact locations of the enzymes have been debated and a detailed phylogenetic 197
analysis suggests the presence of a fourth enzyme type in the endoplasmic reticulum (ER) 198
(Dorion and Rivoal, 2015). The NDPKs are multi-substrate enzymes accepting all nucleoside / 199
deoxynucleoside diphosphates (Zrenner et al., 2006) but there is a preference for generating 200
GTP (Kihara et al., 2011), which in the chloroplast may assist in repairing photosystem II 201
(Spetea and Lundin, 2012). Mutation of the gene for the plastidic NDPK in rice results in a 202
pale green phenotype and a lower photosynthetic rate (Zhou et al., 2017; Ye et al., 2016), 203
but since the chloroplast function is partially retained, there must be also nucleoside 204
triphosphate import into this organelle. Interestingly, NDPKs can also have moonlighting 205
activity as modulators of gene expression (Dorion and Rivoal, 2018). 206
Besides nucleotides, the nucleus and organelles need deoxynucleotides (dNTPs) for DNA 207
synthesis. Deoxynucleotide synthesis requires the reduction of the hydroxyl moiety on the 208
2’ carbon of the ribose by an enzyme complex called ribonucleotide reductase (RNR, Figure 209
4, #10). The RNR complex is comprised of two large regulatory (R1) and two small catalytic 210
(R2) subunits. Mutation of the major R2 subunit gene (tso2) results in lower dNTP 211
concentrations and abnormal plant development, while the additional mutation of a further 212
R2 subunit gene (Arabidopsis has three R2 subunit genes in total) is lethal (Wang and Liu, 213
2006). The substrates of RNR are the ribonucleotide diphosphates, suggesting that for CTP a 214
dedicated phosphatase might exist to support dCDP synthesis (Figure 4A). Alternatively, CDP 215
for dCTP synthesis might be generated from salvage of cytidine (see below). Interestingly, 216 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by
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RNR is subject to a complex allosteric regulation to adjust the correct dNTP pool sizes 217
(Sauge-Merle et al., 1999). In plants, RNR resides exclusively in the cytosol with the potential 218
to relocate to the nucleus upon exposure to UV radiation (Lincker et al., 2004). Especially 219
the plastidic DNA replication seems to rely strongly on sufficient RNR activity, because 220
partially compromising the function of the large RNR subunit by different mutations in the 221
corresponding gene resulted in reduced dNTP levels and impaired chloroplast division in 222
Arabidopsis (Garton et al., 2007). Consistently, chlorophyll biosynthesis in rice is reduced in 223
mutants of the small RNR subunit genes (Chen et al., 2015). All dNDPs can be synthesized 224
directly by RNR, except thymidine diphosphate, because it has no ribonucleotide 225
counterpart. Instead, RNR catalyzes the formation of dUDP from UDP (Figure 4B) and dUMP 226
is methylated at C5 to TMP catalyzed by thymidilate synthase. In Arabidopsis, three 227
enzymes were recently characterized as thymidylate synthases, which are also dihydrofolate 228
reductases (DHFR-TS, Figure 4B, #15) with only two isoforms displaying thymidylate 229
synthase activity (Gorelova et al., 2017). Interestingly, in roots all isoforms can reside either 230
in the cytosol, the nucleus, or the mitochondria depending on the developmental state of 231
the cell, but not in plastids. The two active isoforms seem to be redundant, since only a 232
double mutant of the respective genes is lethal, whereas single gene loss-of-function 233
mutants are phenotypically inconspicuous (Gorelova et al., 2017). The substrate for DHAFR-234
TS is dUMP (Gorelova et al., 2017), but the RNR provides dUDP. It is unknown which enzyme 235
links these two processes in vivo. An alternative dUMP source in mitochondria is the 236
deamination of dCMP as shown recently in rice (Niu et al., 2017; Xu et al., 2014). 237
238
SALVAGE AND DEGRADATION 239
Metabolic sources of nucleosides and nucleobases 240
Nucleosides and nucleobases can be released from nucleotides or nucleic acids in 241
metabolism (Figures 2, 5 and 6) or can be taken up from the environment (Girke et al., 242
2014), where they can occur in substantial amounts (Phillips et al., 1997). 243
The main metabolic source for most nucleosides is probably the turnover of RNA, in 244
particular in the vacuole. Vacuolar RNA degradation, for example of ribosomal RNA after 245
ribophagy (Floyd et al., 2015), generates nucleotides which likely are degraded to 246
nucleosides by vacuolar phosphatases. The details of this process have not been 247 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
and the other three deoxynucleosides, respectively. 279
Several salvage enzymes have a critical function for plant metabolism and their mutation 280
has severe consequences. Mutation of the gene for the main APRT (Figure 5, #19) activity, 281
APT1 (At1g27450), results in male sterility (Gaillard et al., 1998b), whereas a strong 282
downregulation increases the resistance to oxidative stress (Sukrong et al., 2012). Deletion 283
or strong downregulation of the gene for the main ADK (Figure 5, #20) enzyme, ADK1 284
(At3g09820), compromises transmethylation reactions, because the accumulating 285
adenosine inhibits S-adenosylhomocystein (SAH) hydrolase – an enzyme of the SAM cycle. It 286
has been shown that ADK1 and SAH hydrolase interact and partially reside in the nucleus 287
probably mediated by nuclear methyltransferases (Lee et al., 2012). Reduced 288
transmethylation causes a range of developmental abnormalities (Young et al., 2006; 289
Moffatt et al., 2002). Guanine and hypoxanthine salvage seems to be less critical, because 290
HGPRT (Figure 5, #21) mutants are phenotypically normal except for a slight delay in 291
germination (Schroeder et al., 2018; Liu et al., 2007). Mutation of HGPRT leads to guanine 292
but not hypoxanthine accumulation in vivo, probably reflecting that guanine can only be 293
salvaged, whereas hypoxanthine can also be degraded (Baccolini and Witte, 2019). Kinase 294
activity for inosine and guanosine has been measured in plant extracts (Deng and Ashihara, 295
2010; Katahira and Ashihara, 2006) (IGK, Figure 5A, #22) but the corresponding gene is still 296
unknown. Some evidence has been provided that the activity is associated with the 297
intermembrane space of mitochondria (Combes et al., 1989). 298
The only uracil salvage activity in Arabidopsis is located in plastids and encoded by UPP 299
(UPRT, Figure 6, #39). Mutation of UPP leads to growth arrest in the seedling stage and an 300
albino phenotype (Mainguet et al., 2009). Interestingly, it was recently shown that this 301
phenotype is unrelated to the lack of UPRT activity in the mutant, but is caused by the 302
absence of the UPP protein per se, demonstrating that uracil salvage does not play such an 303
essential role for Arabidopsis as previously thought (Ohler et al., 2019). Salvage of uridine is 304
more prominent than salvage of uracil in Arabidopsis. Uridine and cytidine salvage are 305
performed by dual-specific uridine and cytidine kinases (UCK) (Ohler et al., 2019). These 306
enzymes also possess a UPRT-like domain, but do not have UPRT activity (Chen and Thelen, 307
2011). Simultaneous mutation of UCK1 and UCK2 results in dwarf plants that fail to reach 308 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
maturity (Chen and Thelen, 2011). Previously, UCK1 and UCK2 were found to localize in 309
plastids (Chen and Thelen, 2011), but Ohler et al. (2019) demonstrated that these enzymes 310
reside in the cytosol, which was also confirmed in our laboratory (M. Chen and C.-P. Witte, 311
unpublished data). 312
Interestingly, deoxynucleoside-specific salvage enzymes also exist (Figure 4) and the 313
abrogation of thymidine salvage by thymidine kinase (TK, Figure 4B, #14) is lethal for plants 314
(Clausen et al., 2012). However, it is unclear, why thymidine salvage is of such importance. 315
Thymidine kinase occurs in the cytosol, the mitochondria, and the plastids (Xu et al., 2015) 316
and is of particular importance for chloroplast maintenance when germinating seedlings 317
turn autotrophic (Pedroza-García et al., 2019). The other deoxynucleosides are salvaged by 318
an enzyme with broad deoxynucleoside specificity (Clausen et al., 2012) (dNK, Figure 4, 319
#11), potentially associated with mitochondria (Clausen et al., 2014). 320
Purine Nucleotide Degradation 321
Instead of being salvaged, nucleobases and nucleosides can also be fully degraded by plants, 322
but for guanine, adenine, and adenosine a salvage reaction needs to precede degradation. 323
Adenine and adenosine first must be converted to AMP, which can then be deaminated by 324
AMP deaminase (AMPD, Figure 5A, #2) to IMP as a first step into degradation. This is 325
necessary because Arabidopsis and plants in general lack adenosine deaminase (Chen et al., 326
2018b; Dancer et al., 1997). Interestingly, for N6-methyl AMP, plants as well as many other 327
eukaryotes possess a special deaminase, called N6-methyl-AMP deaminase (MAPDA) (Chen 328
et al., 2018b). N6-methylated adenine is the most frequent modification in mRNA, but is 329
also present in other RNA species (Chen and Witte, 2019). MAPDA is phylogenetically 330
related to adenosine deaminases and hydrolyzes N6-methyl AMP to IMP removing the 331
aminomethyl group. This example shows that modified nucleotides must also have an 332
access route to general nucleotide degradation. 333
From IMP, the purine nucleotide degradation pathway cannot be entered directly in 334
Arabidopsis, but conversion to XMP and apparently even to GMP is required (Baccolini and 335
Witte, 2019). These recent results show that the route for AMP catabolism and the route for 336
GMP biosynthesis (partially) overlap. Therefore, branch points of both routes must be 337
controlled, but it is not yet clear how this is achieved. GMP dephoshorylation by a so far 338
unknown phosphatase (GMPP, Figure 5A, #23) initiates purine nucleotide catabolism. At the 339 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
stage of guanosine, salvage back to the nucleotide level via IGK (Figure 5A, #22) is still 340
possible, but the GMPP and IGK reactions might be spatially or temporarily separated to 341
avoid a futile cycle. The deamination of guanosine to xanthosine by guanosine deaminase 342
(GSDA, Figure 5A, #24; Dahncke and Witte, 2013) marks the point of no return, because 343
xanthosine cannot be salvaged and is dedicated for degradation (Yin et al., 2014). Although 344
xanthosine appears to be generated mainly by GSDA, there is strong evidence for an 345
alternative route directly from XMP to xanthosine catalyzed by an XMP phosphatase (XMPP, 346
Figure 5A, #25) (Baccolini and Witte, 2019). An XMP-specific phosphatase, which may 347
represent this XMPP, is currently under investigation in our laboratory. In summary, GMP 348
catabolism begins with dephosphorylation and deamination of guanosine, and most AMP is 349
apparently also degraded via GMP, while some might be dephosphorylated already at the 350
stage of XMP. 351
In clear contrast to purine metabolism in many other organisms, guanine is not an 352
intermediate of purine nucleotide catabolism in Arabidopsis and probably most plants. For 353
degradation, guanine must first be salvaged to GMP (Dahncke and Witte, 2013; Baccolini 354
and Witte, 2019). As well in contrast to purine metabolism in many other organisms, inosine 355
and hypoxanthine are not major intermediates of purine nucleotide catabolism in 356
Arabidopsis, because they are not derived from IMP dephosphorylation (Baccolini and 357
Witte, 2019), but possibly from t-RNA turnover and base excision repair of deaminated 358
adenine in DNA (Figure 5A). Because guanine and hypoxanthine do not play an important 359
role in purine nucleotide degradation, HGPRT (Figure 5A, #21) is decoupled from purine 360
catabolism in plants (Baccolini and Witte, 2019), which is in stark contrast to humans, where 361
mutation of HGPRT results in accumulation of purine nucleotide breakdown products and 362
severe phenotypic consequences (Lesch-Nyhan Syndrome) (Torres and Puig, 2007). 363
Purine catabolism can lead to the complete disintegration of the purine ring in plants 364
(Werner and Witte, 2011) (Figure 5B) to recycle nitrogen (Soltabayeva et al., 2018), but is 365
also used to generate the intermediates uric acid and especially allantoin, which counteract 366
stress by reducing reactive oxygen species (Brychkova et al., 2008; Irani and Todd, 2016; 367
Irani and Todd, 2018; Nourimand and Todd, 2019; Lescano et al., 2016; Watanabe et al., 368
2014; Casartelli et al., 2019; Ma et al., 2016). Sometimes also the accumulation of allantoate 369
has been observed (Alamillo et al., 2010). In tropical legumes like soybean (Glycine max) or 370 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
common bean (Phaseolus vulgaris), the ureides allantoin and allantoate are used as long 371
distance nitrogen transport compounds for the export of fixed nitrogen from the nodules 372
(Carter and Tegeder, 2016; Tegeder, 2014) mediated by the ureide permease (UPS) 373
transporters (Collier and Tegeder, 2012; Desimone et al., 2002; Schmidt et al., 2006). 374
Ureides also function in long distance transport in non-nodulated legumes (Diaz-Leal et al., 375
2012; Quiles et al., 2019) and are probably used in many plants for this purpose (Redillas et 376
al., 2019; Lescano et al., 2016). 377
It has recently been shown that xanthosine hydrolysis to xanthine and ribose is catalyzed by 378
a cytosolic nucleoside hydrolase heteromer consisting of nucleoside hydrolase 1 (NSH1, 379
Figure 5A, #26) and nucleoside hydrolase 2 (NSH2, Figure 5A, #27) in vivo (Baccolini and 380
Witte, 2019). NSH1 has only weak xanthosine and inosine but strong uridine hydrolase 381
activity (Jung et al., 2009; Jung et al., 2011; Baccolini and Witte, 2019; Riegler et al., 2011). 382
However, NSH1 is required to activate NSH2, which is the stronger xanthosine and inosine 383
hydrolase in the complex. Nucleoside catabolism is the major metabolic source of ribose, 384
which is recycled to ribose-5-phosphate by ribokinase in the plastids (Riggs et al., 2016; 385
Schroeder et al., 2018). Xanthine and hypoxanthine are catabolized by the same enzyme, 386
xanthine dehydrogenase (XDH, Figure 5A, #28; Urarte et al., 2015) finally to uric acid in the 387
cytosol. Arabidopsis has a second gene encoding XDH (At4g34900) with no apparent 388
xanthine dehydrogenase activity in vivo (Hauck et al., 2014). Interestingly, XDH has been 389
shown to play a dual role during powdery mildew pathogen attack on Arabidopsis (Ma et al., 390
2016). In the epidermis the enzyme is postulated to operate as an NADH oxidase generating 391
superoxide (Zarepour et al., 2010) to prevent fungal entry, whereas in the mesophyll it 392
works as a xanthine dehydrogenase producing urate, which is suggested to function as a 393
reactive oxygen species scavenger. It was proposed that by this mechanism the reactive 394
oxygen species are confined to the infection site. For further degradation, uric acid must be 395
imported into the peroxisomes, but molecular details about this import are still unknown. In 396
the peroxisome, urate is oxidized by urate oxidase (UOX, Figure 5B, #29) as well as 397
hydrolyzed and decarboxylated by allantoin synthase (ALNS, Figure 5B, #30) to (S)-allantoin 398
(Lamberto et al., 2010; Pessoa et al., 2010). Mutation of UOX leads to strong accumulation 399
of uric acid, which is deleterious for peroxisome maintenance in the embryo, leading to a 400
severe suppression of germination and seedling establishment (Hauck et al., 2014) – 401 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
surprisingly, accumulation of similar amounts of xanthine in Arabidopsis plants lacking XDH 402
does not lead to strong phenotypic alterations under standard growth conditions (Hauck et 403
al., 2014; Schroeder et al., 2018; Soltabayeva et al., 2018). Allantoin must be transported 404
from the peroxisomes to the ER for further degradation, but it is unclear how this is 405
achieved. One may speculate that allantoin accumulation under certain stress conditions 406
may be in part caused by altered peroxisome to ER transport efficiency. However, one 407
apparent reason for allantoin accumulation is an altered catalytic capacity for allantoin 408
generation and degradation under stress (Irani and Todd, 2016; Irani and Todd, 2018; 409
Lescano et al., 2016; Casartelli et al., 2019). 410
In the ER, allantoin is hydrolyzed by four enzymes (Figure 5B, #31 to #34) completely 411
releasing the ring nitrogen as ammonia (Werner et al., 2008; Werner et al., 2010; Serventi et 412
al., 2010; Todd and Polacco, 2006). These enzymes are also responsible for supplying the 413
shoot of tropical legumes with nitrogen exported from the nodules as allantoin and 414
allantoate (Werner et al., 2013; Díaz-Leal et al., 2014). 415
Pyrimidine Nucleotide Degradation 416
Pyrimidine nucleotide catabolism is initiated by UMP / CMP phosphatase(s) (UCPP, Figure 6, 417
#36) which have not yet been identified. Their activity might be temporarily and / or 418
spatially separated from uridine cytidine kinases (UCKs, Figure 6, #35; Ohler et al., 2019) to 419
avoid a futile cycle of pyrimidine nucleotide dephosphorylation and pyrimidine nucleoside 420
salvage. Cytidine is deaminated to uridine by a cytosolic cytidine deaminase (CDA, Figure 6, 421
#37). Interestingly, plants can neither degrade nor salvage the free base cytosine (Katahira 422
and Ashihara, 2002). Arabidopsis contains several copies of cytidine deaminase, but only 423
one copy is functional. The mutation of CDA results in smaller plants probably because 424
cytidine accumulation is toxic (Chen et al., 2016). Generally, the accumulation of nucleosides 425
can reduce plant performance as has been shown for GSDA (Figure 5A, #24) mutants 426
(Schroeder et al., 2018). Consistently, transgenic lines with increased vacuolar nucleoside 427
export (Bernard et al., 2011) are smaller than the wild type. 428
Uridine is hydrolyzed by the cytosolic nucleoside hydrolase 1 (NSH1, Figure 6, #26) to uracil 429
and ribose (Jung et al., 2009). NSH2 is not involved in uridine hydrolysis. NSH1 occurs in two 430
forms in vivo, either as a homomer (probably a homodimer: Kopecná et al., 2013) for uridine 431
hydrolysis, and as a heteromer interacting with NSH2 for xanthosine and inosine hydrolysis 432 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
(Baccolini and Witte, 2019). One should note that these nucleoside hydrolases usually do 433
not hydrolyze cytidine (Jung et al., 2009) or guanosine in vivo unless these compounds 434
accumulate in catabolic mutants (Chen et al., 2016; Dahncke and Witte, 2013; Baccolini and 435
Witte, 2019). Adenosine is a substrate of NSH1 and also of 5′-methylthioadenosine 436
nucleosidase 2 (MTAN2; Siu et al., 2008) in vitro, but both enzymes hydrolyze adenosine 437
with very low catalytic efficiency. The main adenosine hydrolytic activity of Arabidopsis 438
resides probably in the apoplast (see below). 439
The plastidic nucleobase transporter (PLUTO, Figure 6, #38) reallocates uracil probably in 440
symport with protons from the cytosol into the plastids for further metabolic conversion 441
(Witz et al., 2012). PLUTO belongs to the Nucleobase:Cation Symporter 1 (NCS1) family and 442
transports guanine and adenine as well, albeit with lower efficiency than uracil. There are 443
indications that a thiamine precursor, hydroxymethylpyrimidine, is also a PLUTO substrate 444
(Beaudoin et al., 2018). Interestingly, it was recently reported that PLUTO orthologs from 445
two grasses do not transport uracil, but only adenine and guanine next to a few other 446
substrates (Rapp et al., 2016), indicating that uracil metabolism might be organized 447
differently in these species. However, one should note that definite evidence for a function 448
of PLUTO in uracil transport into plastids in vivo has not yet been presented in any plant. 449
Other transporters capable of uracil transport have been identified, but these are located in 450
the plasma membrane (Niopek-Witz et al., 2014; Schmidt et al., 2004). 451
In the plastid, there is a branch point: uracil can either be salvaged by UPRT (Figure 6, #39, 452
see above) or be degraded. When uracil is applied from outside, strong catabolic activity is 453
usually observed (Ashihara et al., 2001; Katahira and Ashihara, 2002). The first reaction, in 454
which the uracil ring is reduced to dihydrouracil by dihydropyrimidine dehydrogenase (DPYD 455
/ PYD1, Figure 5, #40) residing in plastids, was shown to be rate limiting (Tintemann et al., 456
1985). Compared to mammalian DPYD, the plant enzyme lacks C-terminal domains for 457
cofactor binding, which are involved in electron delivery to the active site. Therefore the 458
plant enzyme is probably incomplete and might require a so far unknown interaction 459
partner for activity. The loss of activity, when the enzyme is expressed in the cytosol instead 460
of the plastid, is in agreement with this hypothesis (Cornelius et al., 2011). Mutants of DPYD 461
/ PYD1 show delayed germination and a misregulation of ABA responsive genes, whereas 462
constitutive overexpression results in an increase in growth and seed number (Cornelius et 463 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
al., 2011). In the next enzymatic steps, the dihydrouracil ring is opened by 464
dihydropyrimidine hydrolase (DPYH / PYD2, Figure 6, #41) and then the carbamino group is 465
hydrolytically released by -ureidopropionase (-UP / PYD3, Figure 6, #42; Walsh et al., 466
2001) generating -alanine. Not only uracil but also 5-methyluracil (thymine) is degraded in 467
this pathway (Cornelius et al., 2011) resulting in -aminoisobutyrate instead of -alanine. 468
The first reaction (DPYD, Figure 6, #40) is located in the plastids, the second (DPYH, Figure 6, 469
#41) in the ER, and the third (-UP, Figure 6, #42) in the cytosol, but it is unclear why such a 470
distribution is favorable, and how the metabolites are shuttled to these different locations 471
(Zrenner et al., 2009). Recently, the combination of genome-wide association data with 472
correlation networks built from metabolite and transcriptome data identified an 473
aminotransferase correlated with -alanine. The corresponding mutants accumulated -474
alanine, indicating that this might be the missing -alanine aminotransferase (BAAT / PYD4, 475
Figure 6, #43) of pyrimidine catabolism in plants (Wu et al., 2016). 476
Pyrimidine catabolism is induced by nitrogen starvation and in senescence (Cornelius et al., 477
2011; Zrenner et al., 2009) suggesting that similar to purine nitrogen also pyrimidine 478
nitrogen is recycled by plants. When uracil is given as the sole nitrogen source, its 479
degradation can support the growth of Arabidopsis to a limited extent (Zrenner et al., 2009). 480
EXTRACELLUAR ATP 481
Extracellular ATP (eATP) is a signal molecule, which is either actively released upon a 482
stimulus by plant cells via exocytosis or transport, or which is derived from damaged cells 483
(Cao et al., 2014) (Figure 7). A plasma-membrane based nucleotide transporter belonging to 484
the mitochondrial carrier family (pmANT1, Figure 7, #44) is involved in ATP export with 485
physiological relevance at least in pollen (Rieder and Neuhaus, 2011). eATP plays a role in 486
stress responses and is perceived by the receptor-like kinase ‘does not respond to 487
nucleotides 1’ (DORN1, Figure 7, #50), which recognizes ATP, GTP, and ADP but not AMP 488
and adenosine (Choi et al., 2014). Interestingly, CTP and NAD are also sensed by plant cells 489
and a potential receptor for NAD has been identified recently (Wang et al., 2017). 490
The ATP signal might be quenched by an apoplastic apyrase (Riewe et al., 2008a), an enzyme 491
which hydrolyzes NTPs or NDPs to NMPs. Seven apyrases are encoded by the Arabidopsis 492
genome (APY1 to APY7) and APY1 and APY2 were believed to represent these extracellular 493 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
enzymes (Lim et al., 2014). However, by scanning the substrate spectra of the apyrases, only 494
APY3 (Figure 7, #45) showed strong activity with ATP (and other NTPs) but also APY5 and 495
APY6 were slightly active with NTPs (Chiu et al., 2015). These apyrases are therefore 496
possible candidates for the apolastic enzymes in Arabidopsis. However, other secreted 497
phosphatases might also be involved, for example members of the unspecific purple acid 498
phosphatases (Del Vecchio et al., 2014; Wang et al., 2011). 499
The AMP resulting from ATP dephosphorylation is hydrolyzed in the apoplast to adenosine 500
by a 5’ nucleotidase (Figure 7, #46). An AMP-specific extracellular 5’ nucleotidase associated 501
to the plasma membrane was purified from peanut (Arachis hypogaea) (Sharma et al., 1986; 502
Gupta and Sharma, 1996), but the corresponding gene has not been identified. Adenosine 503
can be either taken up via the adenosine proton symporter ‘equilibrative nucleoside 504
transporter 3’ (ENT3, Figure 7, #47) (Cornelius et al., 2012; Traub et al., 2007) or further 505
hydrolyzed by the apoplastic purine-specific nucleoside hydrolase 3 (NSH3, Figure 7, #48) 506
(Jung et al., 2011) to adenine and ribose. NSH3 hydrolyzes inosine more efficiently than 507
adenosine, whereas a cell wall bound nucleoside hydrolase of potato, probably the ortholog 508
of NSH3 in this plant, was highly specific for adenosine and did not hydrolyze inosine (Riewe 509
et al., 2008b). 510
Simultaneous genetic blockage of nucleoside uptake and hydrolysis leads to an 511
accumulation of adenosine and uridine in the apoplast, a reduction of photosystem II 512
efficiency, and a higher susceptibility to the necrotrophic fungus Botrytis cinerea possibly 513
caused by reduced expression of WRKY33 (Daumann et al., 2015), known to be essential for 514
Botrytis resistance (Liu et al., 2015). Treatment with eATP increases the resistance to 515
Botrytis (Tripathi et al., 2017) and the expression of WRKY33 and other defense related 516
genes is reduced in a dorn1 mutant and boosted in a DORN1 overexpression line upon 517
challenge with eATP (Jewell et al., 2019). Taken together it appears that adenosine 518
accumulation in the apoplast dampens the DORN1 mediated response, indicating that ENT3 519
and NSH3 are required to remove the breakdown products of eATP signaling. Also the 520
adenine resulting from adenosine hydrolysis by NSH3 is taken up by plant cells. It is not 521
entirely clear which transporters mediate this uptake. Possible candidates are azaguanine 522
resistant 1 and 2 (AZG1 and 2; Figure 7, #49), which have been shown to facilitate adenine 523
and guanine uptake into Arabidopsis seedlings (Mansfield et al., 2009), or members of the 524 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
nucleobase-ascorbate transporter (NAT) family (Niopek-Witz et al., 2014) as well as of the 525
purine permease (PUP) family (Girke et al., 2014). Interestingly, fungi seem to be able to 526
influence the purinergic signaling in the apoplast by interfering with apoplastic nucleotide 527
metabolism via the excretion of nucleotidases to improve colonization (Nizam et al., 2019). 528
CONNECTIONS TO CYTOKININ HOMEOSTASIS 529
The biosynthesis of the cytokinins involves the generation of N6-modified AMP, carrying an 530
isoprenoid group (Sakakibara, 2005). However, cytokinin ribotides or ribosides are inactive – 531
the free modified base is the active hormone binding to the receptors (Romanov et al., 532
2018; Yamada et al., 2001). The question arises whether the enzymes that are employed for 533
cytokinin homeostasis (activation from ribotides and inactivation to ribosides / ribotides) 534
are the same as for the metabolism of adenine nucleotides. 535
It was shown that a cytokinin ribotide-specific enzyme (cytokinin riboside 5′-536
monophosphate phosphoribohydrolase, called lonely guy (LOG)) can release the active 537
cytokinin from the ribotide (Kurakawa et al., 2007; Kuroha et al., 2009). A recent report 538
demonstrated that the mutation of the seven genes coding for functional LOGs in 539
Arabidopsis resulted in a phenotype that cannot be attenuated by exogenous cytokinin 540
ribotides, suggesting that the hydrolysis by LOGs is the main pathway of cytokinin activation 541
(Osugi et al., 2017). Therefore, the cytosolic nucleoside hydrolases do not seem to be 542
involved in cytokinin activation, although it could be shown that cytokinin ribosides are 543
substrates in vitro, catalyzed with comparatively low efficiency (Kopecná et al., 2013; Jung 544
et al., 2009). Consistently, cytokinin-related phenotypes were not observed in nucleoside 545
hydrolase mutants (Riegler et al., 2011). However, long-distance transport of cytokinins may 546
involve an activation of cytokinin ribosides / ribotides in the apoplast prior to uptake or 547
perception (Romanov et al., 2018). In Arabidopsis, a third nucleoside hydrolase (NSH3) that 548
is located in the apoplast (see section on extracellular ATP) has been shown to hydrolyze 549
adenosine, but cytokinin ribosides have not been assessed (Jung et al., 2011). Interestingly, 550
an apoplastic nucleoside phosphorylase was isolated from potato that converted cytokinin 551
ribosides to cytokinins and ribose-1-phosphate in the presence of phosphate, and can also 552
work in the synthesis direction of ribosides (Bromley et al., 2014). The enzyme preferred 553
cytokinins / cytokinin ribosides over adenine / adenosine as substrates and is supposedly 554
involved in cytokinin-mediated tuber endodormancy. Close homologs in Arabidopsis (e.g. 555 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
aminotransferase. 661 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Carter AM, Tegeder M (2016) Increasing nitrogen fixation and seed development in soybean 716
requires complex adjustments of nodule nitrogen metabolism and partitioning processes. 717
Current Biol 26: 2044–2051. 718
Casartelli A, Melino VJ, Baumann U, Riboni M, Suchecki R, Jayasinghe NS, Mendis H, 719
Watanabe M, Erban A, Zuther E, Hoefgen R, Roessner U, Okamoto M, Heuer S (2019) 720
Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in 721
bread wheat. Plant Mol Biol 99: 477–497. 722
Chen F, Dong G, Ma X, Wang F, Zhang Y, Xiong E, Wu J, Wang H, Qian Q, Wu L, Yu Y (2018a) 723
UMP kinase activity is involved in proper chloroplast development in rice. Photosynth Res 724
137: 53–67. 725
Chen M, Herde M, Witte C-P (2016) Of the nine cytidine deaminase-like genes in 726
Arabidopsis, eight are pseudogenes and only one is required to maintain pyrimidine 727
homeostasis in vivo. Plant Physiol 171: 799–809. 728
Chen M, Urs MJ, Sánchez-González I, Olayioye MA, Herde M, Witte C-P (2018b) m6A RNA 729
degradation products are catabolized by an evolutionarily conserved N6-Methyl-AMP 730
deaminase in plant and mammalian cells. Plant Cell 30: 1511–1522. 731
Chen M, Witte C-P (2019) Functions and Dynamics of Methylation in Eukaryotic mRNA. In S 732
Jurga, J Barciszewski, eds, The DNA, RNA, and Histone Methylomes. Springer 733
International Publishing, Cham, pp. 333–351.Chen MJ, Thelen JJ (2011) Plastid uridine 734 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Ma X, Wang W, Bittner F, Schmidt N, Berkey R, Zhang L, King H, Zhang Y, Feng J, Wen Y, 906
Tan L, Li Y, Zhang Q, Deng Z, Xiong X, Xiao S (2016) Dual and opposing roles of xanthine 907
dehydrogenase in defense-associated reactive oxygen species metabolism in Arabidopsis. 908
Plant Cell 28: 1108–1126. 909
Mainguet SE, Gakiere B, Majira A, Pelletier S, Bringel F, Guerard F, Caboche M, Berthome 910
R, Renou JP (2009) Uracil salvage is necessary for early Arabidopsis development. Plant J 911
60: 280–291. 912
Mansfield TA, Schultes NP, Mourad GS (2009) AtAzg1 and AtAzg2 comprise a novel family 913
of purine transporters in Arabidopsis. FEBS Lett 583: 481–486. 914
Moffatt B, Ashihara H (2002) Purine and pyrimdine nucleotide synthesis and metabolism, 915
The Arabidopsis book. American Society of Plant Biologists, Rockville, MD. 916 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Chabouté M-E, Devic M (2008) The first zygotic division in Arabidopsis requires de novo 982
transcription of thymidylate kinase. Plant J 53: 776–789. 983
Sabina RL, Paul AL, Ferl RJ, Laber B, Lindell SD (2007) Adenine nucleotide pool perturbation 984
is a metabolic trigger for AMP deaminase inhibitor-based herbicide toxicity. Plant Physiol 985
143: 1752–1760. 986
Sakakibara H (2005) Cytokinin biosynthesis and regulation. Vitam Horm 72: 271–287. 987
Sauge-Merle S, Falconet D, Fontecave M (1999) An active ribonucleotide reductase from 988
Arabidopsis thaliana - Cloning, expression and characterization of the large subunit. Eur J 989
Biochem 266: 62–69. 990 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Traub M, Florchinger M, Piecuch J, Kunz HH, Weise-Steinmetz A, Deitmer JW, Neuhaus HE, 1054
Mohlmann T (2007) The fluorouridine insensitive 1 (fur1) mutant is defective in 1055
equilibrative nucleoside transporter 3 (ENT3), and thus represents an important 1056
pyrimidine nucleoside uptake system in Arabidopsis thaliana. Plant J 49: 855–864. 1057
Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K (2017) Extracellular ATP acts on jasmonate 1058
signaling to reinforce plant defense. Plant Physiol 176: 511–523. 1059
Ullrich A, Knecht W, Piskur J, Loffler M (2002) Plant dihydroorotate dehydrogenase differs 1060
significantly in substrate specificity and inhibition from the animal enzymes. FEBS Lett 1061
529: 346–350. 1062
Urarte E, Esteban R, Moran JF, Bittner F (2015) Established and proposed roles of xanthine 1063
oxidoreductase in oxidative and reductive pathways in plants. In KJ Gupta, AU 1064 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Young LS, Harrison BR, Narayana, M. U. M., Moffatt BA, Gilroy S, Masson PH (2006) 1121
Adenosine kinase modulates root gravitropism and cap morphogenesis in arabidopsis. 1122
Plant Physiol 142: 564–573. 1123
Zarepour M, Kaspari K, Stagge S, Rethmeier R, Mendel RR, Bittner F (2010) Xanthine 1124
dehydrogenase AtXDH1 from Arabidopsis thaliana is a potent producer of superoxide 1125
anions via its NADH oxidase activity. Plant Mol Biol 72: 301–310. 1126
Zhang T, Feng P, Li Y, Yu P, Yu G, Sang X, Ling Y, Zeng X, Li Y, Huang J, Zhang T, Zhao F, 1127
Wang N, Zhang C, Yang Z, Wu R, He G (2018) VIRESCENT-ALBINO LEAF 1 regulates leaf 1128
colour development and cell division in rice. J Exp Bot 69: 4791–4804. 1129
Zhang X, Chen Y, Lin X, Hong X, Zhu Y, Li W, He W, An F, Guo H (2013) Adenine 1130
phosphoribosyl transferase 1 is a key enzyme catalyzing cytokinin conversion from 1131
nucleobases to nucleotides in Arabidopsis. Mol Plant 6: 1661–1672. 1132
Zhou K, Xia J, Wang Y, Ma T, Li Z (2017) A Young Seedling Stripe2 phenotype in rice is 1133
caused by mutation of a chloroplast-localized nucleoside diphosphate kinase 2 required 1134
for chloroplast biogenesis. Genet Mol Biol 40: 630–642. 1135
Zhou L, Lacroute F, Thornburg R (1998) Cloning, expression in Escherichia coli, and 1136
characterization of Arabidopsis thaliana UMP/CMP kinase. Plant Physiol 117: 245–254. 1137 https://plantphysiol.orgDownloaded on January 29, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
• The pathways of plant nucleotide metabolism have been better defined through the detailed analyses of mutants and the discovery of many new genes / proteins involved, for example the plastid uracil transporter, the nucleoside hydrolases, the CTP synthases, and guanosine deaminase.
• It has become clear that purine nucleotide catabolism may not only be involved in recycling nitrogen, but also in producing catabolic intermediates which dampen stress responses.
• Extracellular ATP has emerged as a new signaling molecule.
• Cells contain many modified nucleotides. A first enzyme for the degradation of a modified nucleotide, N6-methyl-AMP, has been discovered.
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• How is nucleotide metabolism regulated (i) on the enzymatic level (ii) by transcriptional and post-transcriptional mechanisms (iii) by compartmentalization or organization in protein complexes (iv) by transport (v) by tissue-specific gene expression?
• Which transporters mediate purine and pyrimidine metabolite movement, specifically (i) catabolic intermediates between different cellular compartments (ii) nucleotides into the organelles (iii) metabolites over long distances?
• How are the nucleotide and deoxynucleotide species in the distinct cellular compartments balanced? Is this adjusted upon developmental and environmental stimuli, and how is this achieved?
• Which nucleotide phosphatases mediate dephosphorylation in vivo, for example dephosphorylation of mononucleotides to nucleosides?
• How are modified and damaged nucleotides degraded, and how do they re-enter nucleotide metabolism?
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Figure 1. Structural composi�on of nucleobases, nucleosides, and nucleo�des.
For the nucleobases ‘R’ is simply a proton. For the nucleosides ‘R’ is a sugar moiety which can be ribose or deoxyribose (carrying a proton instead of a hydroxyl group at the 2’ carbon of the ribose). Nucleo�des have up to three phosphate groups esterified to the hydroxyl group of the 5’ carbon of the nucleoside sugar determining the prefix mono- di- and triphosphate in the name of the molecule. The terminal phosphate always carries two charges irrespec�ve of the number of phosphates present. The pyrimidine nucleobases (upper row) and the purine nucleobases (lower row) are shown with the groups a�ached to the heterocycles highlighted in red (oxo groups), blue (amino groups), and grey shading (methyl group).
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Figure 2. Schema�c overview of plant nucleo�de metabolism.
Nucleo�des are synthesized ‘de novo’ from precursor molecules listed in the upper le� box. The phosphoryla�on of nucleoside monophosphates via nucleoside diphosphates (NDPs) generates nucleoside triphosphates (NTPs), which serve as building blocks for RNA synthesis and as precursors for the biosynthesis of the metabolites shown in the center (S-adenosyl methionine, UDP-glucose, and NADH are given as examples). However, the nucleoside triphosphates, in par�cular ATP and GTP, are not only precursors for other metabolites, but are also essen�al stores of chemical energy in the phosphoanhydride bonds used in a mul�tude of energe�c coupling reac�ons, as well as important donors of phosphate in kinase reac�ons (not shown). NDPs can be reduced to dNDPs (deoxynucleoside diphosphates), which a�er phosphoryla�on to dNTPs serve as precursors for DNA biosynthesis. RNA degrada�on in the cytosol releases nucleoside monophosphates, whereas nucleosides are produced during vacuolar RNA degrada�on. Adenosine and adenine are products of biochemical reac�ons involving S-adenosyl methionine (SAM). Non-enzyma�c decay (depurina�on) and enzyma�c repair reac�ons result in nucleoside and nucleobase release from DNA. Nucleobases and nucleosides can be recycled to nucleo�des in so called ‘salvage’ reac�ons. Plants are also capable of full nucleo�de degrada�on via certain nucleosides and nucleobases releasing the nitrogen of the nucleobases as ammonia.
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Figure 4. Synthesis of nucleoside and deoxynucleoside triphosphates. 1
Synthesis of (A) cy�dylates, (B) uridylates and thymidylates, (C) guanylates, and (D) 2 adenylates. RNR (10), ribonucleo�de reductase; dNK (11), deoxynucleoside kinase; UMK (12), 3 UMP kinase; NDPK (13), nucleoside diphosphate kinase; TK (14), thymidine kinase; DHFR-TS 4 (15), dihydrofolate reductase-thymidylate synthase; TMK (16), thymidylate kinase; GMK (17), 5 guanylate kinase; AMK (18), adenylate kinase. The subcellular loca�ons where enzymes with 6 these ac�vi�es are found are indicated. For TMK, a loca�on in the plas�ds is only assumed. 7 The mononucleo�des (AMP, GMP, UMP, and CMP) may also be derived from salvage 8 reac�ons (see Figures 5 and 6). 9
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Parsed CitationsAlamillo JM, Diaz-Leal JL, Sanchez-Moran MV, Pineda M (2010) Molecular analysis of ureide accumulation under drought stress inPhaseolus vulgaris L. Plant Cell Environ 33: 1828–1837.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ashihara H, Loukanina N, Stasolla C, Thorpe TA (2001) Pyrimidine metabolism during somatic embryo development in white spruce(Picea glauca). J Plant Physiol 158: 613–621.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ashihara H, Stasolla C, Fujimura T, Crozier A (2018) Purine salvage in plants. Phytochemistry 147: 89–124.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Atkins CA, Shelp BJ, Storer PJ (1985) Purification and properties of inosine monophosphate oxidoreductase from nitrogen-fixingnodules of cowpea (Vigna-Unguiculata-L WALP). Arch Biochem Biophys 236: 807–814.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Atkins CA, Smith, P. M. C., Storer PJ (1997) Reexamination of the intracellular localization of de novo purine synthesis in cowpeanodules. Plant Physiol 113: 127–135.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Baccolini C, Witte C-P (2019) AMP and GMP catabolism in Arabidopsis converge on xanthosine, which is degraded by a nucleosidehydrolase heterocomplex. Plant Cell 31: 734–751.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bahaji A, Muñoz FJ, Ovecka M, Baroja-Fernández E, Montero M, Li J, Hidalgo M, Almagro G, Sesma MT, Ezquer I, Pozueta-Romero J(2011a) Specific delivery of AtBT1 to mitochondria complements the aberrant growth and sterility phenotype of homozygous Atbt1Arabidopsis mutants. Plant J 68: 1115–1121.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bahaji A, Ovecka M, Bárány I, Risueño MC, Muñoz FJ, Baroja-Fernández E, Montero M, Li J, Hidalgo M, Sesma MT, Ezquer I, TestillanoPS, Pozueta-Romero J (2011b) Dual targeting to mitochondria and plastids of AtBT1 and ZmBT1, two members of the mitochondrialcarrier family. Plant Cell Physiol 52: 597–609.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Barbado C, Cordoba-Canero D, Arizaa RR, Roldan-Arjona T (2018) Nonenzymatic release of N7-methylguanine channels repair ofabasic sites into an AP endonuclease-independent pathway in Arabidopsis. Proc Natl Acad Sci USA 115: E916-E924.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Beaudoin GAW, Johnson TS, Hanson AD (2018) The PLUTO plastidial nucleobase transporter also transports the thiamin precursorhydroxymethylpyrimidine. Biosci Rep 38.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bernard C, Traub M, Kunz HH, Hach S, Trentmann O, Mohlmann T (2011) Equilibrative nucleoside transporter 1 (ENT1) is critical forpollen germination and vegetative growth in Arabidopsis. J Exp Bot 62: 4627–4637.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bromley JR, Warnes BJ, Newell CA, Thomson JCP, James CM, Turnbull CGN, Hanke DE (2014) A purine nucleoside phosphorylase inSolanum tuberosum L. (potato) with specificity for cytokinins contributes to the duration of tuber endodormancy. Biochem J 458: 225–237.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Brychkova G, Alikulov Z, Fiuhr R, Sagi M (2008) A critical role for ureides in dark and senescence-induced purine remobilization isunmasked in the Atxdh1 Arabidopsis mutant. Plant J 54: 496–509.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Cao Y, Tanaka K, Nguyen CT, Stacey G (2014) Extracellular ATP is a central signaling molecule in plant stress responses. Curr OpinPlant Biol 20: 82–87.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Carrari F, Coll-Garcia D, Schauer N, Lytovchenko A, Palacios-Rojas N, Balbo I, Rosso M, Fernie AR (2005) Deficiency of a plastidialadenylate kinase in Arabidopsis results in elevated photosynthetic amino acid biosynthesis and enhanced growth. Plant Physiol 137:70–82.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Carter AM, Tegeder M (2016) Increasing nitrogen fixation and seed development in soybean requires complex adjustments of nodulenitrogen metabolism and partitioning processes. Current Biol 26: 2044–2051.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Casartelli A, Melino VJ, Baumann U, Riboni M, Suchecki R, Jayasinghe NS, Mendis H, Watanabe M, Erban A, Zuther E, Hoefgen R,Roessner U, Okamoto M, Heuer S (2019) Opposite fates of the purine metabolite allantoin under water and nitrogen limitations inbread wheat. Plant Mol Biol 99: 477–497.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen F, Dong G, Ma X, Wang F, Zhang Y, Xiong E, Wu J, Wang H, Qian Q, Wu L, Yu Y (2018a) UMP kinase activity is involved in properchloroplast development in rice. Photosynth Res 137: 53–67.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen M, Herde M, Witte C-P (2016) Of the nine cytidine deaminase-like genes in Arabidopsis, eight are pseudogenes and only one isrequired to maintain pyrimidine homeostasis in vivo. Plant Physiol 171: 799–809.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen M, Urs MJ, Sánchez-González I, Olayioye MA, Herde M, Witte C-P (2018b) m6A RNA degradation products are catabolized by anevolutionarily conserved N6-Methyl-AMP deaminase in plant and mammalian cells. Plant Cell 30: 1511–1522.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen M, Witte C-P (2019) Functions and Dynamics of Methylation in Eukaryotic mRNA. In S Jurga, J Barciszewski, eds, The DNA, RNA,and Histone Methylomes. Springer International Publishing, Cham, pp. 333–351.Chen MJ, Thelen JJ (2011) Plastid uridine salvageactivity is required for photoassimilate allocation and partitioning in Arabidopsis. Plant Cell 23: 2991–3006.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chen X, Zhu L, Xin L, Du K, Ran X, Cui X, Xiang Q, Zhang H, Xu P, Wu X (2015) Rice stripe1-2 and stripe1-3 mutants encoding the smallsubunit of ribonucleotide reductase are temperature sensitive and are required for chlorophyll biosynthesis. PloS One 10: e0130172.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Chiu T-Y, Lao J, Manalansan B, Loqué D, Roux SJ, Heazlewood JL (2015) Biochemical characterization of Arabidopsis apyrase familyreveals their roles in regulating endomembrane NDP/NMP homoeostasis. Biochem J 472: 43–54.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science343: 290–294.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Clausen AR, Girandon L, Ali A, Knecht W, Rozpedowska E, Sandrini MP, Andreasson E, Munch-Petersen B, Piskur J (2012) Twothymidine kinases and one multisubstrate deoxyribonucleoside kinase salvage DNA precursors in Arabidopsis thaliana. FEBS J 279:3889–3897.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Collier R, Tegeder M (2012) Soybean ureide transporters play a critical role in nodule development, function and nitrogen export.Plant J 72: 355–367.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Combes A, Lafleuriel J, Lefloch F (1989) The Inosine-Guanosine Kinase-Activity of Mitochondria in Tubers of Jerusalem Artichoke.Plant Physiol Biochem 27: 729–736.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Cornelius S, Traub M, Bernard C, Salzig C, Lang P, Mohlmann T (2012) Nucleoside transport across the plasma membrane mediated byequilibrative nucleoside transporter 3 influences metabolism of Arabidopsis seedlings. Plant Biol 14: 696–705.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Cornelius S, Witz S, Rolletschek H, Mohlmann T (2011) Pyrimidine degradation influences germination seedling growth and productionof Arabidopsis seeds. J Exp Bot 62: 5623–5632.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dahncke K, Witte CP (2013) Plant purine nucleoside catabolism employs a guanosine deaminase required for the generation ofxanthosine in Arabidopsis. Plant Cell 25: 4101–4109.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dancer JE, Hughes RG, Lindell SD (1997) Adenosine-5'-phosphate deaminase. A novel herbicide target. Plant Physiol 114: 119–129.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Daumann M, Fischer M, Niopek-Witz S, Girke C, Möhlmann T (2015) Apoplastic nucleoside accumulation in Arabidopsis leads toreduced photosynthetic performance and increased susceptibility against Botrytis cinerea. Front Plant Sci 6: 1158.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Daumann M, Hickl D, Zimmer D, DeTar RA, Kunz H-H, Möhlmann T (2018) Characterization of filament-forming CTP synthases fromArabidopsis thaliana. Plant J: 96: 316–328.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Del Vecchio HA, Ying S, Park J, Knowles VL, Kanno S, Tanoi K, She Y-M, Plaxton WC (2014) The cell wall-targeted purple acidphosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J 80: 569–581.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Deng WW, Ashihara H (2010) Profiles of purine metabolism in leaves and roots of Camellia sinensis seedlings. Plant Cell Physiol 51:2105–2118.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Desimone M, Catoni E, Ludewig U, Hilpert M, Schneider A, Kunze R, Tegeder M, Frommer WB, Schumacher K (2002) A novelsuperfamily of transporters for allantoin and other oxo derivatives of nitrogen heterocyclic compounds in Arabidopsis. Plant Cell 14:847–856.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Diaz-Leal JL, Galvez-Valdivieso G, Fernandez J, Pineda M, Alamillo JM (2012) Developmental effects on ureide levels are mediated bytissue-specific regulation of allantoinase in Phaseolus vulgaris L. J Exp Bot 63: 4095–4106.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Díaz-Leal JL, Torralbo F, Antonio Quiles F, Pineda M, Alamillo JM (2014) Molecular and functional characterization of allantoateamidohydrolase from Phaseolus vulgaris. Physiol Plant 152: 43–58.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dong Q, Zhang Y-X, Zhou Q, Liu Q-E, Chen D-B, Wang H, Cheng S-H, Cao L-Y, Shen X-H (2019) UMP Kinase Regulates ChloroplastDevelopment and Cold Response in Rice. Int J Mol Sci 20: 2107.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Doremus HD, Jagendorf AT (1985) Subcellular localization of the pathway of de novo pyrimidine nucleotide biosynthesis in pea leaves.Plant Physiol 79: 856–861.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dorion S, Rivoal J (2015) Clues to the functions of plant NDPK isoforms. Naunyn-Schmiedeberg's Arch Pharmacol 388: 119–132.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dorion S, Rivoal J (2018) Plant nucleoside diphosphate kinase 1: A housekeeping enzyme with moonlighting activity. Plant SignalBehav 13: e1475804.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Feng X, Yang R, Zheng X, Zhang F (2012) Identification of a novel nuclear-localized adenylate kinase 6 from Arabidopsis thaliana as an
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
essential stem growth factor. Plant Physiol Biochem 61: 180–186.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Floyd BE, Morriss SC, MacIntosh GC, Bassham DC (2015) Evidence for autophagy-dependent pathways of rRNA turnover inArabidopsis. Autophagy 11: 2199–2212.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gaillard C, Moffatt BA, Blacker M, Laloue M (1998a) Male sterility associated with APRT deficiency in Arabidopsis thaliana results froma mutation in the gene APT1. Mol Gen Genet 257: 348–353.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gaillard C, Moffatt BA, Blacker M, Laloue M (1998b) Male sterility associated with APRT deficiency in Arabidopsis thaliana results froma mutation in the gene APT1. Mol Gen Genet 257: 348–353.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Garton S, Knight H, Warren GJ, Knight MR, Thorlby GJ (2007) Crinkled leaves 8 - a mutation in the large subunit of ribonucleotidereductase - leads to defects in leaf development and chloroplast division in Arabidopsis thaliana. Plant J 50: 118–127.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Girke C, Daumann M, Niopek-Witz S, Möhlmann T (2014) Nucleobase and nucleoside transport and integration into plant metabolism.Front Plant Sci 5: 443.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gorelova V, Lepeleire J de, van Daele J, Pluim D, Meï C, Cuypers A, Leroux O, Rébeillé F, Schellens JHM, Blancquaert D, Stove CP,van der Straeten D (2017) Dihydrofolate reductase/thymidylate synthase fine-tunes the folate status and controls redox homeostasis inplants. Plant cell 29: 2831–2853.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gupta A, Sharma CB (1996) Purification to homogeneity and characterization of plasma membrane and Golgi apparatus-specific 5'-adenosine monophosphatases from peanut cotyledons. Plant Sci 117: 65–74.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Han BW, Bingman CA, Mahnke DK, Bannen RM, Bednarek SY, Sabina RL, Phillips GN (2006) Membrane association, mechanism ofaction, and structure of Arabidopsis embryonic factor 1 (FAC1). J Biol Chem 81: 14939–14947.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH (2017) SUBA4: the interactive data analysis centre for Arabidopsissubcellular protein locations. Nucleic Acids Res 45: D1064-D1074.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hu D, Li Y, Jin W, Gong H, He Q, Li Y (2017) Identification and characterization of a plastidic adenine nucleotide uniporter (OsBT1-3)required for chloroplast development in the early leaf stage of rice. Sci Rep 7.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Irani S, Todd CD (2016) Ureide metabolism under abiotic stress in Arabidopsis thaliana. J Plant Physiol 199: 87–95.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Irani S, Todd CD (2018) Exogenous allantoin increases Arabidopsis seedlings tolerance to NaCl stress and regulates expression ofoxidative stress response genes. J Plant Physiol 221: 43–50.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ito J, Batth TS, Petzold CJ, Redding-Johanson AM, Mukhopadhyay A, Verboom R, Meyer EH, Millar AH, Heazlewood JL (2011) Analysisof the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J Proteome Res 10: 1571-1582.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jewell JB, Sowders JM, He R, Willis MA, Gang DR, Tanaka K (2019) Extracellular ATP Shapes a Defense-Related Transcriptome Both
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Independently and along with Other Defense Signaling Pathways. Plant Physiol 179: 1144–1158.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jung B, Florchinger M, Kunz HH, Traub M, Wartenberg R, Jeblick W, Neuhaus HE, Mohlmann T (2009) Uridine-ribohydrolase is a keyregulator in the uridine degradation pathway of Arabidopsis. Plant Cell 21: 876–891.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jung B, Hoffmann C, Mohlmann T (2011) Arabidopsis nucleoside hydrolases involved in intracellular and extracellular degradation ofpurines. Plant J 65: 703–711.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kafer C, Zhou L, Santoso D, Guirgis A, Weers B, Park S, Thornburg R (2004) Regulation of pyrimidine metabolism in plants. FrontBiosci-Landmrk 9: 1611–1625.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Karran P, Lindahl T (1980) Hypoxanthine in deoxyribonucleic acid: generation by heat-induced hydrolysis of adenine residues andrelease in free form by a deoxyribonucleic acid glycosylase from calf thymus. Biochem 19: 6005–6011.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Katahira R, Ashihara H (2002) Profiles of pyrimidine biosynthesis, salvage and degradation in disks of potato (Solanum tuberosum L.)tubers. Planta 215: 821–828.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Katahira R, Ashihara H (2006) Profiles of purine biosynthesis, salvage and degradation in disks of potato (Solanum tuberosum L.)tubers. Planta 225: 115–126.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kihara A, Saburi W, Wakuta S, Kim M-H, Hamada S, Ito H, Imai R, Matsui H (2011) Physiological and biochemical characterization ofthree nucleoside diphosphate kinase isozymes from rice (Oryza sativa L.). Biosci Biotechnol Biochem 75: 1740–1745.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kirchberger S, Tjaden J, Neuhaus HE (2008) Characterization of the Arabidopsis Brittle1 transport protein and impact of reducedactivity on plant metabolism. Plant J 56: 51–63.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kopecná M, Blaschke H, Kopecny D, Vigouroux A, Koncitíková R, Novák O, Kotland O, Strnad M, Moréra S, Schwartzenberg K von(2013) Structure and function of nucleoside hydrolases from Physcomitrella patens and maize catalyzing the hydrolysis of purine,pyrimidine, and cytokinin ribosides. Plant Physiol 163: 1568–1583.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kumar V, Spangenberg O, Konrad M (2000) Cloning of the guanylate kinase homologues AGK-1 and AGK-2 from Arabidopsis thalianaand characterization of AGK-1. Eur J Biochem 267: 606–615.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristemactivity by a cytokinin-activating enzyme. Nature 445: 652 EP -.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses ofLONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21: 3152–3169.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lamberto I, Percudani R, Gatti R, Folli C, Petrucco S (2010) Conserved alternative splicing of Arabidopsis transthyretin-like determinesprotein localization and S-allantoin synthesis in peroxisomes. Plant Cell 22: 1564–1574.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lange PR, Geserick C, Tischendorf G, Zrenner R (2008) Functions of chloroplastic adenylate kinases in Arabidopsis. Plant Physiol 146:492–504.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Google Scholar: Author Only Title Only Author and Title
Lee S, Doxey AC, McConkey BJ, Moffatt BA (2012) Nuclear targeting of methyl-recycling enzymes in Arabidopsis thaliana is mediated byspecific protein interactions. Mol Plant 5: 231–248.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Leroch M, Kirchberger S, Haferkamp I, Wahl M, Neuhaus HE, Tjaden J (2005) Identification and characterization of a novel plastidicadenine nucleotide uniporter from Solanum tuberosum. J Biol Chem 280: 17992–18000.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lescano CI, Martini C, González CA, Desimone M (2016) Allantoin accumulation mediated by allantoinase downregulation and transportby ureide permease 5 confers salt stress tolerance to Arabidopsis plants. Plant Mol Biol 91: 581-595
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lim MH, Wu J, Yao J, Gallardo IF, Dugger JW, Webb LJ, Huang J, Salmi ML, Song J, Clark G, Roux SJ (2014) Apyrase suppressionraises extracellular ATP levels and induces gene expression and cell wall changes characteristic of stress responses. Plant Physiol164: 2054–2067.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lincker F, Philipps G, Chabouté M-E (2004) UV-C response of the ribonucleotide reductase large subunit involves both E2F-mediatedgene transcriptional regulation and protein subcellular relocalization in tobacco cells. Nucleic Acids Res 32: 1430–1438.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Liu S, Kracher B, Ziegler J, Birkenbihl RP, Somssich IE (2015) Negative regulation of ABA signaling by WRKY33 is critical forArabidopsis immunity towards Botrytis cinerea. eLife 4: e07295.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Liu XY, Qian WQ, Liu X, Qin HJ, Wang DW (2007) Molecular and functional analysis of hypoxanthine-guanine phosphoribosyltransferasefrom Arabidopsis thaliana. New Phytol 175: 448–461.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Luzarowski M, Kosmacz M, Sokolowska E, Jasinska W, Willmitzer L, Veyel D, Skirycz A (2017) Affinity purification with metabolomic andproteomic analysis unravels diverse roles of nucleoside diphosphate kinases. J Exp Bot 68: 3487–3499.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ma X, Wang W, Bittner F, Schmidt N, Berkey R, Zhang L, King H, Zhang Y, Feng J, Wen Y, Tan L, Li Y, Zhang Q, Deng Z, Xiong X, Xiao S(2016) Dual and opposing roles of xanthine dehydrogenase in defense-associated reactive oxygen species metabolism in Arabidopsis.Plant Cell 28: 1108–1126.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Mainguet SE, Gakiere B, Majira A, Pelletier S, Bringel F, Guerard F, Caboche M, Berthome R, Renou JP (2009) Uracil salvage isnecessary for early Arabidopsis development. Plant J 60: 280–291.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Mansfield TA, Schultes NP, Mourad GS (2009) AtAzg1 and AtAzg2 comprise a novel family of purine transporters in Arabidopsis. FEBSLett 583: 481–486.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Moffatt B, Ashihara H (2002) Purine and pyrimdine nucleotide synthesis and metabolism, The Arabidopsis book. American Society ofPlant Biologists, Rockville, MD.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Moffatt B, Pethe C, Laloue M (1991) Metabolism of benzyladenine is impaired in a mutant of Arabidopsis thaliana lacking adeninephosphoribosyltransferase activity. Plant Physiol 95: 900–908.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Moffatt BA, Stevens YY, Allen MS, Snider JD, Pereira LA, Todorova MI, Summers PS, Weretilnyk EA, Martin-McCaffrey L, Wagner C(2002) Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation. Plant Physiol 128:812–821.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Niopek-Witz S, Deppe J, Lemieux MJ, Möhlmann T (2014) Biochemical characterization and structure-function relationship of two plantNCS2 proteins, the nucleobase transporters NAT3 and NAT12 from Arabidopsis thaliana. Biochim Biophys Acta 1838: 3025–3035.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Niu M, Wang Y, Wang C, Lyu J, Wang Y, Dong H, Long W, Di Wang, Kong W, Wang L, Guo X, Sun L, Hu T, Zhai H, Wang H, Wan J (2017)ALR encoding dCMP deaminase is critical for DNA damage repair, cell cycle progression and plant development in rice. J Exp Bot 68:5773–5786.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nizam S, Qiang X, Wawra S, Nostadt R, Getzke F, Schwanke F, Dreyer I, Langen G, Zuccaro A (2019) Serendipita indica E5′NTmodulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization. EMBO Rep 20: e47430.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nomura Y, Izumi A, Fukunaga Y, Kusumi K, Iba K, Watanabe S, Nakahira Y, Weber APM, Nozawa A, Tozawa Y (2014) Diversity inguanosine 3',5'-bisdiphosphate (ppGpp) sensitivity among guanylate kinases of bacteria and plants. J Biol Chem 289: 15631–15641.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nourimand M, Todd CD (2019) There is a direct link between allantoin concentration and cadmium tolerance in Arabidopsis. PlantPhysiol Biochem 135: 441–449.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ohler L, Niopek-Witz S, Mainguet SE, Möhlmann T (2019) Pyrimidine salvage: physiological functions and interaction with chloroplastbiogenesis. Plant Physiol 180: 1816–1828
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Osugi A, Kojima M, Takebayashi Y, Ueda N, Kiba T, Sakakibara H (2017) Systemic transport of trans-zeatin and its precursor havediffering roles in Arabidopsis shoots. Nat Plants 3: 17112.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pedroza-García J-A, Nájera-Martínez M, Mazubert C, Aguilera-Alvarado P, Drouin-Wahbi J, Sánchez-Nieto S, Gualberto JM, Raynaud C,Plasencia J (2019) Role of pyrimidine salvage pathway in the maintenance of organellar and nuclear genome integrity. Plant J 97: 430–446.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pessoa J, Sarkany Z, Ferreira-da-Silva F, Martins S, Almeida MR, Li JM, Damas AM (2010) Functional characterization of Arabidopsisthaliana transthyretin-like protein. BMC Plant Biol 10: 30.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Phillips DA, Joseph CM, Hirsch PR (1997) Occurrence of flavonoids and nucleosides in agricultural soils. Appl Environ Microbiol 63:4573–4577.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Quiles FA, Galvez-Valdivieso G, Guerrero-Casado J, Pineda M, Piedras P (2019) Relationship between ureidic/amidic metabolism andantioxidant enzymatic activities in legume seedlings. Plant Physiol Biochem 138: 1–8.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rapp M, Schein J, Hunt KA, Nalam V, Mourad GS, Schultes NP (2016) The solute specificity profiles of nucleobase cation symporter 1(NCS1) from Zea mays and Setaria viridis illustrate functional flexibility. Protoplasma 253: 611–623.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Redillas MCFR, Bang SW, Lee D‐K, Kim YS, Jung H, Chung PJ, Suh J‐W, Kim J‐K (2019) Allantoin accumulation throughoverexpression of ureide permease1 improves rice growth under limited nitrogen conditions. Plant Biotechnol J 17: 1289–1301.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Regierer B, Fernie AR, Springer F, Perez-Melis A, Leisse A, Koehl K, Willmitzer L, Geigenberger P, Kossmann J (2002) Starch contentand yield increase as a result of altering adenylate pools in transgenic plants. Nat Biotechnol 20: 1256–1260.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rieder B, Neuhaus HE (2011) Identification of an Arabidopsis plasma membrane-located ATP transporter important for antherdevelopment. Plant Cell 23: 1932–1944.
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riegler H, Geserick C, Zrenner R (2011) Arabidopsis thaliana nucleosidase mutants provide new insights into nucleoside degradation.New Phytol 191: 349–359.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riewe D, Grosman L, Fernie AR, Wucke C, Geigenberger P (2008a) The potato-specific apyrase is apoplastically localized and hasinfluence on gene expression, growth, and development. Plant Physiol 147: 1092–1109.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riewe D, Grosman L, Fernie AR, Zauber H, Wucke C, Geigenberger P (2008b) A cell wall-bound adenosine nucleosidase is involved inthe salvage of extracellular ATP in Solanum tuberosum. Plant Cell Physiol 49: 1572–1579.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riggs JW, Rockwell NC, Cavales PC, Callis J (2016) Identification of the plant ribokinase and discovery of a role for Arabidopsisribokinase in nucleoside metabolism. J Biol Chem 291: 22572–22582.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Romanov GA, Lomin SN, Schmülling T (2018) Cytokinin signaling: from the ER or from the PM? That is the question! New Phytol 218:41–53.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ronceret A, Gadea-Vacas J, Guilleminot J, Lincker F, Delorme V, Lahmy S, Pelletier G, Chabouté M-E, Devic M (2008) The first zygoticdivision in Arabidopsis requires de novo transcription of thymidylate kinase. Plant J 53: 776–789.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sabina RL, Paul AL, Ferl RJ, Laber B, Lindell SD (2007) Adenine nucleotide pool perturbation is a metabolic trigger for AMP deaminaseinhibitor-based herbicide toxicity. Plant Physiol 143: 1752–1760.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sakakibara H (2005) Cytokinin biosynthesis and regulation. Vitam Horm 72: 271–287.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sauge-Merle S, Falconet D, Fontecave M (1999) An active ribonucleotide reductase from Arabidopsis thaliana - Cloning, expressionand characterization of the large subunit. Eur J Biochem 266: 62–69.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sauter M, Moffatt B, Saechao MC, Hell R, Wirtz M (2013) Methionine salvage and S-adenosylmethionine: essential links betweensulfur, ethylene and polyamine biosynthesis. Biochem J 451: 145–154.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmid L-M, Ohler L, Möhlmann T, Brachmann A, Muiño JM, Leister D, Meurer J, Manavski N (2019) PUMPKIN, the sole plastid UMPkinase, associates with group II introns and alters their metabolism. Plant Physiol 179: 248–264.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmidt A, Baumann N, Schwarzkopf A, Frommer WB, Desimone M (2006) Comparative studies on ureide permeases in Arabidopsisthaliana and analysis of two alternative splice variants of AtUPS5. Planta 224: 1329–1340.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmidt A, Su YH, Kunze R, Warner S, Hewitt M, Slocum RD, Ludewig U, Frommer WB, Desimone M (2004) UPS1 and UPS2 fromArabidopsis mediate high affinity transport of uracil and 5-fluorouracil. J Biol Chem 279: 44817–44824.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I (2003) Structure and function of cytokinin oxidase/dehydrogenasegenes of maize, rice, Arabidopsis and other species. J Plant Res 116: 241–252.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schoor S, Farrow S, Blaschke H, Lee S, Perry G, Schwartzenberg K von, Emery N, Moffatt B (2011) Adenosine kinase contributes tocytokinin interconversion in Arabidopsis. Plant Physiol 157: 659–672.
Pubmed: Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Google Scholar: Author Only Title Only Author and Title
Schroeder RY, Zhu A, Eubel H, Dahncke K, Witte C-P (2018) The ribokinases of Arabidopsis thaliana and Saccharomyces cerevisiae arerequired for ribose recycling from nucleotide catabolism, which in plants is not essential to survive prolonged dark stress. New Phytol217: 233–244.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Serventi F, Ramazzina I, Lamberto I, Puggioni V, Gatti R, Percudani R (2010) Chemical basis of nitrogen recovery through the ureidepathway. Formation and hydrolysis of S-ureidoglycine in plants and bacteria. ACS Chem Biol 5: 203–214.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sharma CB, Mittal R, Tanner W (1986) Purification and properties of a glycoprotein adenosine 5′-monophosphatase from the plasmamembrane fraction of Arachis hypogaea cotyledons. Biochim Biophys Acta 884: 567–577.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Shelp BJ, Atkins CA (1983) Role of Inosine monophosphate oxidoreductase in the formation of ureides in nitrogen-fixing nodules ofcowpea (Vigna-unguiculata-L Walp). Plant Physiol 72: 1029–1034.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sigel H, Operschall BP, Griesser R (2009) Xanthosine 5 '-monophosphate (XMP). Acid-base and metal ion-binding properties of achameleon-like nucleotide. Chem Soc Rev 38: 2465–2494.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Siu KKW, Lee JE, Sufrin JR, Moffatt BA, McMillan M, Cornell KA, Isom C, Howell PL (2008) Molecular determinants of substratespecificity in plant 5'-methylthioadenosine nucleosidases. J Mol Biol 378: 112–128.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smith PM, Atkins CA (2002) Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol 128: 793–802.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Soltabayeva A, Srivastava S, Kurmanbayeva A, Bekturova A, Fluhr R, Sagi M (2018) Early senescence in older leaves of low nitrate-grown Atxdh1 uncovers a role for purine catabolism in N supply. Plant Physiol 178: 1027–1044.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Spetea C, Lundin B (2012) Evidence for nucleotide-dependent processes in the thylakoid lumen of plant chloroplasts-an update. FEBSLett 586: 2946–2954.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stasolla C, Katahira R, Thorpe TA, Ashihara H (2003) Purine and pyrimidine nucleotide metabolism in higher plants. J Plant Physiol 160:1271–1295.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stitt M, Lilley RM, Heldt HW (1982) Adenine-nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts.Plant Physiol 70: 971–977.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sugimoto H, Kusumi K, Noguchi K, Yano M, Yoshimura A, Iba K (2007) The rice nuclear gene, VIRESCENT 2, is essential for chloroplastdevelopment and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. Plant J 52: 512–527.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides. Opportunities for cropimprovement. J Exp Bot 65: 1865–1878.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tintemann H, Wasternack C, Benndorf R, Reinbothe H (1985) The rate-limiting step of uracil degradation in tomato cell-suspensioncultures and Euglena-gracilis invivo studies. Comp Biochem Physiol, Part B: Biochem Mol Biol 82: 787–792.
Pubmed: Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Traub M, Florchinger M, Piecuch J, Kunz HH, Weise-Steinmetz A, Deitmer JW, Neuhaus HE, Mohlmann T (2007) The fluorouridineinsensitive 1 (fur1) mutant is defective in equilibrative nucleoside transporter 3 (ENT3), and thus represents an important pyrimidinenucleoside uptake system in Arabidopsis thaliana. Plant J 49: 855–864.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K (2017) Extracellular ATP acts on jasmonate signaling to reinforce plant defense. PlantPhysiol 176: 511–523.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ullrich A, Knecht W, Piskur J, Loffler M (2002) Plant dihydroorotate dehydrogenase differs significantly in substrate specificity andinhibition from the animal enzymes. FEBS Lett 529: 346–350.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Urarte E, Esteban R, Moran JF, Bittner F (2015) Established and proposed roles of xanthine oxidoreductase in oxidative and reductivepathways in plants. In KJ Gupta, AU Igamberdiev, eds, Reactive oxygen and nitrogen species signaling and communication in plants.Springer, Cham, Switzerland, pp. 15–42.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wagner KG, Backer AI (1992) Dynamics of nucleotides in plants studied on a cellular basis. In JK W, F M, eds, International Review ofCytology Vol. 134, pp. 1–84.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Walsh TA, Green SB, Larrinua IM, Schmitzer PR (2001) Characterization of plant beta-ureidopropionase and functional overexpressionin Escherichia coli. Plant Physiol 125: 1001–1011.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu JW,Wang D, Liu D (2011) The Arabidopsis purple acid phosphataseAt-PAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. PlantPhysiol 157: 1283–1299.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wang C, Liu Z (2006) Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plantdevelopment. Plant Cell 18: 350–365.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wang C, Zhou M, Zhang X, Yao J, Zhang Y, Mou Z (2017) A lectin receptor kinase as a potential sensor for extracellular nicotinamideadenine dinucleotide in Arabidopsis thaliana. eLife 6: e25474
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Watanabe S, Matsumoto M, Hakomori Y, Takagi H, Shimada H, Sakamoto A (2014) The purine metabolite allantoin enhances abioticstress tolerance through synergistic activation of abscisic acid metabolism. Plant Cell Environ 37: 1022–1036.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wei X, Song X, Wei L, Tang S, Sun J, Hu P, Cao X (2017) An epiallele of rice AK1 affects photosynthetic capacity. J Integr Plant Biol 59:158–163.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Werner AK, Medina-Escobar N, Zulawski M, Sparkes IA, Cao F-Q, Witte CP (2013) The ureide-degrading reactions of purine ringcatabolism employ three amidohydrolases and one aminohydrolase in Arabidopsis, soybean, and rice. Plant Physiol 163: 672–681.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Werner AK, Romeis T, Witte CP (2010) Ureide catabolism in Arabidopsis thaliana and Escherichia coli. Nat Chem Biol 6: 19–21.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Werner AK, Sparkes IA, Romeis T, Witte CP (2008) Identification, biochemical characterization, and subcellular localization of allantoateamidohydrolases from Arabidopsis and soybean. Plant Physiol 146: 418–430.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Werner AK, Witte CP (2011) The biochemistry of nitrogen mobilization: purine ring catabolism. Trends Plant Sci 16: 381–387.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Witz S, Jung B, Furst S, Mohlmann T (2012) De novo pyrimidine nucleotide synthesis mainly occurs outside of plastids, but a previouslyundiscovered nucleobase importer provides substrates for the essential salvage pathway in Arabidopsis. Plant Cell 24: 1549–1559.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wu S, Alseekh S, Cuadros-Inostroza A, Fusari CM, Mutwil M, Kooke R, Keurentjes JB, Fernie AR, Willmitzer L, Brotman Y (2016)Combined use of genome-wide association data and correlation networks unravels key regulators of primary metabolism inArabidopsis thaliana. PLoS GENET 12.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Xu J, Deng Y, Li Q, Zhu X, He Z (2014) STRIPE2 encodes a putative dCMP deaminase that plays an important role in chloroplastdevelopment in rice. J Genet Genomics 41: 539–548.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Xu J, Zhang HY, Xie CH, Xue HW, Dijkhuis P, Liu CM (2005) EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential forthe zygote to embryo transition in Arabidopsis. Plant J 42: 743–756.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Xu J, Zhang L, Yang D-L, Li Q, He Z (2015) Thymidine kinases share a conserved function for nucleotide salvage and play an essentialrole in Arabidopsis thaliana growth and development. New Phytol 208: 1089–1103.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is acytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42: 1017–1023.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ye W, Hu S, Wu L, Ge C, Cui Y, Chen P, Wang X, Xu J, Ren D, Dong G, Qian Q, Guo L (2016) White stripe leaf 12 (WSL12), encoding anucleoside diphosphate kinase 2 (OsNDPK2), regulates chloroplast development and abiotic stress response in rice (Oryza sativa L.).Mol Breeding 36: 57.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yin Y, Katahira R, Ashihara H (2014) Metabolism of purine nucleosides and bases in suspension-cultured Arabidopsis thaliana cells.Eur Chem Bull 3: 925–934.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Young LS, Harrison BR, Narayana, M. U. M., Moffatt BA, Gilroy S, Masson PH (2006) Adenosine kinase modulates root gravitropism andcap morphogenesis in arabidopsis. Plant Physiol 142: 564–573.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zarepour M, Kaspari K, Stagge S, Rethmeier R, Mendel RR, Bittner F (2010) Xanthine dehydrogenase AtXDH1 from Arabidopsisthaliana is a potent producer of superoxide anions via its NADH oxidase activity. Plant Mol Biol 72: 301–310.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhang T, Feng P, Li Y, Yu P, Yu G, Sang X, Ling Y, Zeng X, Li Y, Huang J, Zhang T, Zhao F, Wang N, Zhang C, Yang Z, Wu R, He G (2018)VIRESCENT-ALBINO LEAF 1 regulates leaf colour development and cell division in rice. J Exp Bot 69: 4791–4804.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhang X, Chen Y, Lin X, Hong X, Zhu Y, Li W, He W, An F, Guo H (2013) Adenine phosphoribosyl transferase 1 is a key enzymecatalyzing cytokinin conversion from nucleobases to nucleotides in Arabidopsis. Mol Plant 6: 1661–1672.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
Zhou K, Xia J, Wang Y, Ma T, Li Z (2017) A Young Seedling Stripe2 phenotype in rice is caused by mutation of a chloroplast-localizednucleoside diphosphate kinase 2 required for chloroplast biogenesis. Genet Mol Biol 40: 630–642.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhou L, Lacroute F, Thornburg R (1998) Cloning, expression in Escherichia coli, and characterization of Arabidopsis thaliana UMP/CMPkinase. Plant Physiol 117: 245–254.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhu X, Guo S, Wang Z, Du Q, Xing Y, Zhang T, Shen W, Sang X, Ling Y, He G (2016) Map-based cloning and functional analysis of YGL8,which controls leaf colour in rice (Oryza sativa). BMC Plant Biol 16: 134.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zrenner R, Ashihara H (2011) Nucleotide Metabolism. In H Ashihara, A Crozier, A Komamine, eds, Plant metabolism and biotechnology.Wiley, Cambridge, New York, pp. 135–162.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zrenner R, Riegler H, Marquard CR, Lange PR, Geserick C, Bartosz CE, Chen CT, Slocum RD (2009) A functional analysis of thepyrimidine catabolic pathway in Arabidopsis. New Phytol 183: 117–132.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57:805–836.
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
https://plantphysiol.orgDownloaded on January 29, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.