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Ann Bot. 2009 April; 103(6): 819–824.
Published online 2009 February 5. doi:  10.1093/aob/mcp019
PMCID: PMC2707885

The role of NAD biosynthesis in plant development and stress responses

Abstract

Background

Pyridine nucleotides are essential for electron transport and serve as co-factors in multiple metabolic processes in all organisms. Each nucleotide has a particular role in metabolism. For instance, the NAD/NADP ratio is believed to be responsible for sustaining the functional status of plant cells. However, since enzymes involved in the synthesis and degradation of NAD and NADP have not been fully identified, the physiological functions of these co-enzymes in plant growth and development are largely unknown.

Scope

This Botanical Briefing covers progress in the developmental and stress-related roles of genes associated with NAD biosynthesis in plants. Special attention will be given to assessments of physiological impacts through the modulation of NAD and NADP biosynthesis.

Conclusions

The significance of NAD biosynthesis in plant development and NADP biosynthesis in plant stress tolerance is summarized in this Briefing. Further investigation of cells expressing a set of NAD biosynthetic genes would facilitate understanding of regulatory mechanisms by which plant cells maintain NAD homeostasis.

Key words: NAD biosynthesis, nicotinate/nicotinamide mononucleotide adenylyltransferase (NMNAT), chloroplastic NADP biosynthesis, NAD kinase 2 (NADK2)

INTRODUCTION

Pyridine nucleotide co-enzymes are essential metabolites for numerous redox reactions in living organisms (Berger et al., 2004; Hunt et al., 2004; Noctor et al., 2006). Nicotinamide adenine dinucleotide (NAD) and its derivative NADP are traditionally known as the central metabolites orchestrating plant cellular redox homeostasis. These nucleotides also play vital roles in signalling via the generation and scavenging of reactive oxygen species (ROS; Mittler et al., 2004) and in systems controlling adaptation to environmental stresses such as UV irradiation, salinity, heat shock and drought (Amor et al., 1998; Chai et al., 2005, 2006). In addition to functional roles in redox regulation, recent evidence suggests new roles for NAD and its derivatives in regulating complex cellular processes, including transcriptional regulation and microtubule metabolism via NAD-dependent deacetylation and/or mono/poly(ADP-ribos)ylation, and intracellular Ca2+ signalling via NAD-derived cyclic ADP-ribose (Imai et al., 2000; North et al., 2003; Sanchez et al., 2004; De Block et al., 2005). These cellular events are accompanied by a decrease in cellular NAD level independently of redox reactions. A by-product of these reactions is free nicotinamide. Interestingly, a deficiency of poly(ADP-ribose) polymerase (PARP) alleviates the NAD decrease and ATP consumption, resulting in enhanced tolerance to drought, heat and high-light stresses (De Block et al., 2005). To avoid cell death due to NAD depletion, plant cells possess a mechanism for maintaining cellular NAD levels, i.e. NAD is immediately re-synthesized when the level is decreased. Recent advances in the characterization of the Arabidopsis NAD biosynthetic genes has shed light on the significance of NAD biosynthesis in various developmental processes, including seed germination and pollen-tube growth (Hashida et al., 2007; Hunt et al., 2007). Unlike a variety of genes encoding NAD catabolic enzymes, the genes responsible for each step of NAD biosynthesis consist of just a single or only a very few copies in the genome of Arabidopsis (Hunt et al., 2004; Noctor et al., 2006).

In this review, we mainly discuss the biological significance of genes associated with NAD and NADP biosynthesis in plants. Special attention will be focused on nicotinate/nicotinamide mononucleotide adenylyltransferase (NMNAT) as a key enzyme in NAD biosynthesis and on NAD kinase 2 (NADK2) as a key enzyme in chloroplastic NADP biosynthesis.

AtNMNAT: A KEY GENE IN NAD BIOSYNTHESIS

Historically, because of the housekeeping role of NAD in the fine-tuning of cellular homeostasis through primary and secondary metabolism, the functional significance and the regulatory mechanisms of NAD biosynthesis have received little attention. Recently, several genes involved in NAD biosynthesis have been identified, as summarized in Fig. 1. In brief, aspartate serves as a precursor in the de-novo synthesis of NAD in Arabidopsis (Katoh et al., 2006). After the formation of quinolinate from aspartate and dihydroxyacetone phosphate by aspartate oxidase plus quinolinate synthase, quinolinate is converted to nicotinate mononucleotide (NaMN) by quinolinate phosphoribosyltransferase. Subsequently, NaMN is converted by adenylylation to nicotinate adenine dinucleotide (NaAD), followed by amidation of NaAD to NAD as the final step of NAD biosynthesis. NAD utilization is shown by thick arrows in Fig. 1. Besides redox reactions, NAD acts as a substrate for (cyclic)ADP-ribose generation, poly(ADP-ribos)ylation, protein deacetylation, and so on, during which processes NAD is broken down to nicotinamide. In combination with the de-novo synthetic pathway, Arabidopsis uses a salvage pathway in which NaMN is formed from nicotinamide through two enzymatic steps (Katoh et al., 2006; Wang and Pichersky, 2007). Since nicotinamide is a product of NAD degradation, the latter case is the so-called NAD recycling system. The nature of plant NAD recycling is quite different from that of mammals because nicotinate synthesis from nicotinamide is absent in mammals (Chappie et al., 2005). In mammals, phosphoribose is transferred directly to the pyridine ring by nicotinamide phosphoribosyltransferase (Revollo et al., 2004; Wang et al., 2006). NAD is then produced from nicotinamide mononucleotide (NMN) by adenylylation. Bifunctional NaMN/NMN adenylyltransferase (NMNAT), which catalyses the conversion both of NaMN to NaAD and of NMN to NAD+, is important in mammals (Raffaelli et al., 2002). Consistently, the catalytic properties of human NMNATs (NMNAT1, NMNAT2 and NMNAT3) and their subcellular compartmentalization have pointed to non-redundant functions in NAD biosynthesis (Berger et al., 2005).

Fig. 1.
Schematic diagram illustrating four possible pathways for NAD biosynthesis. The diagram summarizes current knowledge on plants, mainly Arabidopsis, and mammals (uniquely the two-step salvage pathway). Arabidopsis produces NaMN using a combination of the ...

There is only one NMNAT-encoding gene in Arabidopsis (At5g55810: AtNMNAT), so that the AtNMNAT gene is responsible for all NAD biosynthesis. Understandably, atnmnat homozygous plants could not be isolated (Hashida et al., 2007), supporting the suggestion that AtNMNAT is indispensable and is a prerequisite for NAD biosynthesis. Other mutant studies have indicated that quinolinate phosphoribosyltransferase (QPT) is also essential in de-novo NAD biosynthesis (Katoh et al., 2006). In addition to the genetic evidence, biochemical analysis also demonstrates the importance of AtNMNAT in NAD biosynthesis. Unlike in mammals, it is still unknown whether the NAD synthetic process from NMN is present or absent in plants. At least, AtNMNAT, like mammalian NMNAT, can also transfer phosphoribose to the pyridine ring of NMN (Hashida et al., 2007). So, if the ‘NMN to NAD pathway’ exists in Arabidopsis, AtNMNAT should be a rate-limiting factor. As described above, the NaMN adenylyltransferase activity contributes to both the de-novo and the four-step recycling pathways in plants. Another salvage pathway remained elusive until the detection of nicotinate riboside (NaR) kinase activity in mung bean seedlings (Matsui and Ashihara, 2008). The discovery of this activity indicates the presence of an alternative synthetic pathway for NaMN from NaR in plants. Thus, the de-novo, salvage and alternative pathways converge onto NaMN synthesis, suggesting the functional importance of AtNMNAT in the plant. Further studies are needed to determine the cellular compartment in which AtNMNAT catalysis occurs, and also to explore whether its enzymatic properties could be influenced by the metabolic profile of NAD and its precursors or products. Comparison of amino acid sequences suggests that the enzymatic properties of AtNMNAT are different from those of individual human NMNATs.

NAD AND NADP BIOSYNTHESIS IN PLANT DEVELOPMENT

Recently, phenotypic analyses of Arabidopsis NAD biosynthetic mutants have emphasized the functional importance of this biosynthesis in plant developmental processes (Hashida et al., 2007; Hunt et al., 2007). A T-DNA insertion loss-of-function atnmnat mutant is lethal but even the heterozygous atnmnat mutant is distinguishable from other NAD biosynthetic mutants based on phenotypic abnormality. Frequent production of shorter siliques due to male gametophytic malfunction suggests an essential role of NAD biosynthesis in pollen fertility. Based on the traditional interpretation of NAD biosynthesis, the pollen mother-cell disperses NAD co-enzymes equally when it generates four microspores. Correspondingly, an AtNMNAT promoter–reporter fusion suggests prominent NAD biosynthesis before microspore separation, most likely during pollen meiosis. In addition, high AtNMNAT promoter activity was shown during pollen maturation (Fig. 2). Since pollen mitosis I generates non-equivalent sister cells (namely, a vegetative cell and a sperm cell that have subtly different cytoplasm), the NAD synthesis in the latter stage is likely to be involved in developing normal cellular function. The atnmnat mutant pollen has a lower NAD content and is unable to elongate its pollen-tube after germination, supporting the suggestion that ongoing NAD biosynthesis is important to pollen development. A number of studies have investigated Arabidopsis pollen development and metabolic regulation. A number of metabolic pathways operating during pollen maturation and tube growth (e.g. the synthesis of lipids, cell wall components and amino acids) are highly dependent on NAD co-enzymes. Recent microarray data indicate the gene expressions of NAD-dependent and NAD-degrading enzymes in pollen (http://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi; Winter et al., 2007). Mammalian poly(ADP-ribose) polymerase associated with prominent NAD biosynthesis is shown to be involved in male gametogenesis and spermiogenesis (Di Meglio et al., 2003; Dantzer et al., 2006). To test whether the model claimed in mammals can be adapted to plants, genetic identification of NAD-degrading enzymes expressed during pollen development would be needed.

Fig. 2.
NAD biosynthesis in different stages of pollen development and growth. The pollen mother-cell (PMC) develops four male gametophytes surrounded by callose (light blue). NAD biosynthesis in the PMC continues until microspore separation by callose degradation, ...

Despite plants having single or only a few copy numbers of genes for the enzymes catalysing the reactions of NAD biosynthesis (Fig. 1), there are a large number of redundant NAD-dependent or NAD-degrading genes in plants. For example, Arabidopsis contains 27 genes encoding Nudix (nucleoside diphosphates linked to some moiety X) hydrolases (AtNudix1 to 27), some of which can catalyse the conversion of NAD to NMN in vitro (Wang et al., 2002; Ogawa et al., 2005). Since most mutants of Nudix hydrolases exhibit no phenotypic differences from the wild type, these genes have redundant functions (Ogawa et al., 2008). Therefore, it is quite difficult to identify genes encoding NAD-degrading enzymes responsible for the maintenance of plant development by use of homology-dependent computational searches. However, the recent characterization of NAD biosynthetic genes can help to define the NAD-degrading genes responsible for particular cellular events, including pollen germination and tube growth. If the NAD-degrading cells require concurrent NAD biosynthesis to prevent NAD depletion, identification of the site expressing the NAD biosynthetic gene will enable determination of the site of NAD-degrading reactions contributing to cellular function. For example, the expression pattern of the nicotinamidase gene, NIC2, has suggested its functional role in salvage synthesis during seed germination (Hunt et al., 2007). Since NAD-degrading, nicotinamide-producing enzymes [e.g. poly(ADP-ribose) polymerases (PARP1, PARP2, PARP3)] in plants could be inhibited by nicotinamide, a lack of NAD recycling in the nic2-1 mutant results in NAD increase. Interestingly, seed germination of the nic2-1 mutant is delayed. Changing the NAD concentration in seeds probably affects an NAD-dependent reaction that is necessary for seed germination. Here, PARP3 is a plausible candidate for an NAD-degrading enzyme because of the similar expression pattern to NIC2. Future studies will elucidate the functional roles of this NAD-degrading enzyme in seed germination, in combination with mutant analysis.

In a recent study, a relationship between NAD levels and the depth of seed dormancy has been reported (Hunt and Gray, 2008). Here, NADP concentration was inversely proportional to NAD concentration and to dormancy, suggesting a fundamental mechanism regulating NAD concentration and/or NAD/NADP ratio by tuning the balance between NADP biosynthesis and NADP catabolism. Genes encoding NADP catabolic enzymes are unknown; however, NAD kinases (NADK1 to 3), which are NADP synthetic enzymes, are well known in Arabidopsis (Fig. 3). NADK1 and NADK3 are located in the cytosol, whereas NADK2 is in the chloroplast (Turner et al., 2004; Berrin et al., 2005; Chai et al., 2005, 2006). A nadk2 mutant showed pale green rosette leaves with growth retardation; however, no morphological or developmental abnormalities were observed in loss-of-function mutants of the cytosolic NAD kinases under standard growth conditions (Chai et al, 2005; Takahashi et al., 2006). The decreased chlorophyll content of the nadk2 mutant may be due to a suppression of NADPH:protochlorophyllide oxidoreductase gene expression, suggesting that NADK2 is a key enzyme in chlorophyll synthesis. NADK2 appears to produce a large amount of NADP in leaves because the mutant exhibits a substantial decrease in total extractable NADK activity. Energy dissipation and zeaxanthin accumulation were increased in the nadk2 mutant, suggesting that depletion of chloroplastic NADPH inhibits zeaxanthin epoxidase activity (Takahashi et al., 2006). Since zeaxanthin epoxidase is involved in abscisic acid (ABA) biosynthesis (Barrero et al., 2005), ABA-related physiological processes such as stomatal movement may be influenced by chloroplastic NADP biosynthesis. Thus, NADK2 appears to be functionally distinct from NADK1 and NADK3 with respect to plant development.

Fig. 3.
Cellular compartmentation of NADKs in plants. Genes for three NADK isoforms, namely, NADK1, NADK2 and NADK3, are reported in Arabidopsis. NADK1 and NADK3 are thought to be cytosolic, whereas NADK2 has been found in the chloroplasts. Dashed lines indicate ...

NAD AND NADP BIOSYNTHESIS IN PLANT STRESS RESPONSES

Besides accumulating evidence on their developmental roles, the NAD-consuming events are traditionally well known to play a part in biotic and abiotic stress responses. Although the mechanisms are still uncertain, the level of poly(ADP-ribose) (PAR) that is synthesized from NAD is proportional to stress severity (Leist et al., 1997; Ha and Snyder, 1999). Interestingly, down-regulation of PARP enhances stress tolerance, possibly owing to a decrease in NAD consumption in the plant (De Block et al., 2005). Reduced NAD consumption may influence plant metabolism and signal transduction. One noteworthy example is an increase in ABA level, which results in induction of several defence-related genes (Vanderauwera et al., 2007). Although Vanderauwera et al. did not report NADP concentrations, NADP(H)-dependent metabolic pathways might have been activated because ABA synthesis is very sensitive to NADP(H)-dependent processes such as zeaxanthin epoxidase (ABA1) and xanthoxin dehydrogenase (ABA2; Gonzalez-Guzman et al., 2002; Barrero et al., 2005). In this respect, Takahashi et al. (2006) confirmed that chloroplast NAD kinase is essential for the proper photosynthetic machinery of PSII and the xanthophyll cycle. Thus, the disturbance of NAD homeostasis shows pleiotropic effects in the response to stresses. Unlike genes responsible for the common pathway in Fig. 1, NAD kinase-encoding genes have distinct functions as described above.

As mentioned earlier, NAD and NADP are essential as co-factors for electron transport and metabolic processes in many organisms. Each nucleotide has a particular role in metabolism: for example, NAD is used primarily in respiratory ATP production whereas NADP is used in reductive biosynthesis. Furthermore, a decrease in the NAD/NADP ratio is tied directly to increasing photosynthetic activity in cyanobacteria (Tamoi et al., 2005). When higher plants are grown under stressful environments, the reduced form of cytosolic NADP (NADPH) is produced in the pentose phosphate pathway by glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase and plays critical roles in the generation of ROS and in the production of anti-oxidants as ROS scavengers. In fact, Arabidopsis NADK1 and NADK3 are inducible by exposure to abiotic stresses such as methyl violgen-induced oxidative stress, high salinity and osmotic shock (Berrin et al., 2005; Chai et al., 2006). In addition, calmodulin (CaM) -dependent NADK activity is known to be enhanced by elicitors such as cellulase, harpin and incompatible bacteria in tobacco suspension cells (Karita et al., 2004) and by cold stress in greenbean (Ruiz et al., 2002). Because a major generator of plant ROS is NADPH-oxidase, increased NADPH can be rate-limiting for ROS production (Murata et al., 2001; Torres et al., 2002). Nonetheless, enhanced sensitivity to ROS stress was observed in NADK-deficient mutants (Berrin et al., 2005; Chai et al., 2005, 2006); also, decreased activity of NADK was observed in response to salinity and drought (Zagdanska, 1990; Delumeau et al., 2000). In conclusion, it is logical to infer that NADP biosynthesis plays an important role in ROS scavenging.

ACKNOWLEDGEMENTS

This research was supported by a Research Fellowship for Young Scientists of JSPS, grants from the Ministry of Agriculture, Forestry and Fisheries, Japan, and CREST, JST, Japan.

LITERATURE CITED

  • Amor Y, Babiychuk E, Inzé D, Levine A. The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Letters. 1998;440:1–7. [PubMed]
  • Barrero JM, Piqueras P, Gonzalez-Guzman M, et al. A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. Journal of Experimental Botany. 2005;56:2071–2083. [PubMed]
  • Berger F, Ramirez-Hernandez MH, Ziegler M. The new life of a centenarian: signalling functions of NAD(P) Trends in Biochemical Science. 2004;29:111–118. [PubMed]
  • Berger F, Lau C, Dahlmann M, Ziegler M. Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. Journal of Biological Chemistry. 2005;280:36334–36341. [PubMed]
  • Berrin JG, Pierrugues O, Brutesco C, et al. Stress induces the expression of AtNADK-1, a gene encoding a NAD(H) kinase in Arabidopsis thaliana. Molecular Genetics and Genomics. 2005;273:10–19. [PubMed]
  • Chai MF, Chen QJ, An R, Chen YM, Chen J, Wang XC. NADK2, an Arabidopsis chloroplastic NAD kinase, plays a vital role in both chlorophyll synthesis and chloroplast protection. Plant Molecular Biology. 2005;59:553–564. [PubMed]
  • Chai MF, Wei PC, Chen QJ, et al. NADK3, a novel cytoplasmic source of NADPH, is required under conditions of oxidative stress and modulates abscisic acid responses in Arabidopsis. Plant Journal. 2006;47:665–674. [PubMed]
  • Chappie JS, Canaves JM, Han GW, Rife CL, Xu Q, Stevens RC. The structure of a eukaryotic nicotinic acid phosphoribosyltransferase reveals structural heterogeneity among type II PRTases. Structure. 2005;13:1385–1396. [PubMed]
  • Dantzer F, Mark M, Quenet D, et al. Poly(ADP-ribose) polymerase-2 contributes to the fidelity of male meiosis I and spermiogenesis. Proceedings of the National Academdy of Science of the USA. 2006;103:14854–14859. [PubMed]
  • De Block M, Verduyn C, De Brouwer D, Cornelissen M. Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant Journal. 2005;41:95–106. [PubMed]
  • Delumeau O, Renard M, Montrichard F. Characterisation and possible redox regulation of the purified calmodulin-dependent NAD+ kinase from Lycopersicon pimpinellifolium. Plant Cell and Environment. 2000;23:1267–1273.
  • Di Meglio S, Denegri M, Vallefuoco S, Tramontano F, Scovassi AI, Quesada P. Poly(ADPR) polymerase-1 and poly(ADPR) glycohydrolase level and distribution in differentiating rat germinal cells. Molecular and Cellular Biochemistry. 2003;248:85–91. [PubMed]
  • Gonzalez-Guzman M, Apostolova N, Belles JM, et al. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell. 2002;14:1833–1846. [PubMed]
  • Ha HC, Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proceedings of the National Academdy of Science of the USA. 1999;96:13978–13982. [PubMed]
  • Hashida SN, Takahashi H, Kawai-Yamada M, Uchimiya H. Arabidopsis thaliana nicotinate/nicotinamide mononucleotide adenyltransferase (AtNMNAT) is required for pollen tube growth. Plant Journal. 2007;49:694–703. [PubMed]
  • Hunt L, Gray JE. The relationship between pyridine nucleotides and seed dormancy. 2008;181:62–70. New Phytologist. [PubMed]
  • Hunt L, Lerner F, Ziegler M. NAD – new roles in signalling and gene regulation in plants. New Phytologist. 2004;163:31–44.
  • Hunt L, Holdsworth MJ, Gray JE. Nicotinamidase activity is important for germination. Plant Journal. 2007;51:341–351. [PubMed]
  • Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000;403:795–800. [PubMed]
  • Karita E, Yamakawa H, Mitsuhara I, Kuchitsu K, Ohashi Y. Three types of tobacco calmodulins characteristically activate plant NAD kinase at different Ca2+ concentrations and pHs. Plant Cell Physiology. 2004;45:1371–1379. [PubMed]
  • Katoh A, Uenohara K, Akita M, Hashimoto T. Early steps in the biosynthesis of NAD in Arabidopsis start with aspartate and occur in the plastid. Plant Physiology. 2006;141:851–857. [PubMed]
  • Leist M, Single B, Kunstle G, Volbracht C, Hentze H, Nicotera P. Apoptosis in the absence of poly-(ADP-ribose) polymerase. Biochemical and Biophysical Research Communications. 1997;233:518–522. [PubMed]
  • Matsui A, Ashihara H. Nicotinate riboside salvage in plants: presence of nicotinate riboside kinase in mungbean seedlings. Plant Physiology and Biochemistry. 2008;46:104–108. [PubMed]
  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends in Plant Science. 2004;9:490–498. [PubMed]
  • Murata Y, Pei ZM, Mori IC, Schroeder J. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001;13:2513–2523. [PubMed]
  • Noctor G, Queval G, Gakiere B. NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. Journal of Experimental Botany. 2006;57:1603–1620. [PubMed]
  • North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Molecular Cell. 2003;11:437–444. [PubMed]
  • Ogawa T, Ueda Y, Yoshimura K, Shigeoka S. Comprehensive analysis of cytosolic Nudix hydrolases in Arabidopsis thaliana. Journal of Biological Chemistry. 2005;280:25277–25283. [PubMed]
  • Ogawa T, Yoshimura K, Miyake H, et al. Molecular characterization of organelle-type Nudix hydrolases in Arabidopsis thaliana. Plant Physiology. 2008;148:1412–1424. [PubMed]
  • Raffaelli N, Sorci L, Amici A, Emanuelli M, Mazzola F, Magni G. Identification of a novel human nicotinamide mononucleotide adenylyltransferase. Biochemical and Biophysical Research Communications. 2002;297:835–840. [PubMed]
  • Revollo JR, Grimm AA, Imai S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. Journal of Biological Chemistry. 2004;279:50754–50763. [PubMed]
  • Ruiz JM, Sanchez E, Garcia PC, Lopez-Lefebre LR, Rivero RM, Romero L. Proline metabolism and NAD kinase activity in greenbean plants subjected to cold-shock. Phytochemistry. 2002;59:473–478. [PubMed]
  • Sanchez JP, Duque P, Chua NH. ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. Plant Journal. 2004;38:381–395. [PubMed]
  • Takahashi H, Watanabe A, Tanaka A, et al. Chloroplast NAD kinase is essential for energy transduction through the xanthophyll cycle in photosynthesis. Plant Cell Physiology. 2006;47:1678–1682. [PubMed]
  • Tamoi M, Miyazaki T, Fukamizo T, Shigeoka S. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant Journal. 2005;42:504–513. [PubMed]
  • Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the USA. 2002;99:517–522. [PubMed]
  • Turner WL, Waller JC, Vanderbeld B, Snedden WA. Cloning and characterization of two NAD kinases from Arabidopsis. identification of a calmodulin binding isoform. Plant Physiology. 2004;135:1243–1255. [PubMed]
  • Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F. Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proceedings of the National Academy of Sciences of the USA. 2007;104:15150–15155. [PubMed]
  • Wang G, Pichersky E. Nicotinamidase participates in the salvage pathway of NAD biosynthesis in Arabidopsis. Plant Journal. 2007;49:1020–1029. [PubMed]
  • Wang S, Mura C, Sawaya MR, Cascio D, Eisenberg D. Structure of a Nudix protein from Pyrobaculum aerophilum reveals a dimer with two intersubunit beta-sheets. Acta Crystallographica, D: Biological Crystallography. 2002;58:571–578. [PubMed]
  • Wang T, Zhang X, Bheda P, Revollo JR, Imai SI, Wolberger C. Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nature Structural and Molecular Biology. 2006;13:661–662. [PubMed]
  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLoS ONE. 2007;2:e718. doi:10.1371/journal.pone.0000718. [PMC free article] [PubMed]
  • Zagdanska B. NAD kinase activity in wheat leaves under water deficit. Acta Biochimica Polonica. 1990;37:385–389. [PubMed]

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