Abstract
Chloroplast-localized NAD kinase (NADK2) is responsible for the production of NADP+, which is an electron acceptor in the linear electron flow of photosynthesis. The Arabidopsis T-DNA-inserted mutant of NADK2 (nadk2) showed delayed growth and pale-green leaves under continuous light conditions. Under short-day conditions (8 h light / 16 h dark), the nadk2 mutant showed more severe growth inhibition.The genomic fragment containing the promoter and coding region of NADK2 complemented the phenotypes of nadk2 obtained under continuous light and short-day conditions. The nadk2 mutant produced higher amounts of H2O2 and O2−, which were reduced in the complementary line. Under short-day conditions, the nadk2 mutant accumulated more H2O2 than under continuous light conditions. The accumulation of ascorbate and up-regulation of the PDF1.2 and PR1 genes indicated that the nadk2 mutant is under ROS stress and responding to keep its living activities.
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Abbreviations
- DAB 3:
-
3-Diaminobenzidine
- H2O2 :
-
Hydrogen peroxide
- NADP:
-
Nicotinamide adenine dinucleotide phosphate
- NAD+ :
-
Nicotinamide adenine dinucleotide
- NBT:
-
Nitro blue tetrazolium chloride
- ROS:
-
Reactive oxygen species
- WT:
-
Wild type
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology, vol. 105. Elsevier, pp 121–126
Alvarez MaE, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784
Apel K, Hier H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Berrin J-G, Pierrugues O, Brutesco C, Alonso B, Montillet J-L, Roby D, Kazmaier M (2005) Stress induces the expression of AtNADK-1, a gene encoding a NAD (H) kinase in Arabidopsis thaliana. Mol Genet Genom 273:10–19
Ceusters N, Valcke R, Frans M, Claes JE, Van den Ende W, Ceusters J (2019) Performance index and PSII connectivity under drought and contrasting light regimes in the CAM orchid Phalaenopsis. Front Plant Sci 10:1012
Chai M-F, Chen Q-J, An R, Chen Y-M, Chen J, Wang X-C (2005) NADK2, an Arabidopsis chloroplastic NAD kinase, plays a vital role in both chlorophyll synthesis and chloroplast protection. Plant Mol Biol 59:553–564
Chai MF, Wei PC, Chen QJ, An R, Chen J, Yang S, Wang XC (2006) NADK3, a novel cytoplasmic source of NADPH, is required under conditions of oxidative stress and modulates abscisic acid responses in Arabidopsis. Plant J 47:665–674
Chassot C, Nawrath C, Métraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49:972–980
Dell’Aglio E, Giustini C, Kraut A, Couté Y, Costa A, Decros G (2019) Identification of the Arabidopsis calmodulin-dependent NAD+ kinase that sustains the elicitor-induced oxidative burst. Plant Physiol 181:1449–1458
Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 06:119–133
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Gakière B, Fernie AR, Pétriacq P (2018) More to NAD+ than meets the eye: a regulator of metabolic pools and gene expression in Arabidopsis. Free Radic Biol Med 122:86–95
Hashida S-N, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot 103:819–824
Hashida S-N, Miyagi A, Nishiyama M, Yoshida K, Hisabori T, Kawai-Yamada M (2018) Ferredoxin/thioredoxin system plays an important role in the chloroplastic NADP status of Arabidopsis. Plant J 95:947–960
Ishikawa Y, Kawai-Yamada M, Hashida S-N (2020) Measurement of chloroplastic NAD kinase activity and whole tissue NAD kinase assay. Bio-Protoc 10:e3480–e3480
Ishikawa Y, Miyagi A, Haishima Y, Ishikawa T, Nagano M, Yamaguchi M, Hihara Y, Kawai-Yamada M (2016) Metabolomic analysis of NAD kinase-deficient mutants of the cyanobacterium Synechocystis sp. PCC 6803. J Plant Physiol 205:105–112
Ji D, Li Q, Guo Y, An W, Manavski N, Meurer J, Chi W (2022) NADP+ supply adjusts the synthesis of photosystem I in Arabidopsis chloroplasts. Plant Physiol 189:2128–2143
Kawai-Yamada M, Miyagi A, Sato Y, Hosoi Y, Hashida S-N, Ishikawa T, Yamaguchi M (2021) Altered metabolism of chloroplastic NAD kinase-overexpressing Arabidopsis in response to magnesium sulfate supplementation. Plant Signal Behav 16:1844509
Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Miyagi A, Takahashi H, Takahara K, Hirabayashi T, Nishimura Y, Tezuka T, Kawai-Yamada M, Uchimiya H (2010) Principal component and hierarchical clustering analysis of metabolites in destructive weeds; polygonaceous plants. Metabolomics 6:146–155
Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 gene. Mol Plant Microbe Interact 23:340–351
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395
Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425
Ohashi K, Kawai S, Koshimizu M, Murata K (2011) NADPH regulates human NAD kinase, a NADP+-biosynthetic enzyme. Mol Cell Biochem 355:57–64
Onda Y, Miyagi A, Takahara K, Uchimiya H, Kawai-Yamada M (2014) Effects of NAD kinase 2 overexpression on primary metabolite profiles in rice leaves under elevated carbon dioxide. Plant Biol 16:819–824
Penninckx I, Eggermont K, Terras FR, Thomma B, De Samblanx GW, Buchala A, Métraux J-P, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323
Pétriacq P, de Bont L, Tcherkez G, Gakière B (2013) NAD: not just a pawn on the board of plant-pathogen interactions. Plant Signal Behav 8:e22477
Pétriacq P, Ton J, Patrit O, Tcherkez G, Gakière B (2016) NAD acts as an integral regulator of multiple defense layers. Plant Physiol 172:1465–1479
Pollak N, Dölle C, Ziegler M (2007) The power to reduce: pyridine nucleotides–small molecules with a multitude of functions. Biochem J 402:205–218
Sim Choi H, Woo Kim J, Cha YN, Kim C (2006) A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoassay Immunochem 27:31–44
Takahara K, Kasajima I, Takahashi H, Hashida S-n, Itami T, Onodera H, Toki S, Yanagisawa S, Kawai-Yamada M, Uchimiya H (2010) Metabolome and photochemical analysis of rice plants overexpressing Arabidopsis NAD kinase gene. Plant Physiol 152:1863–1873
Takahashi H, Takahara K, Hashida S-N, Hirabayashi T, Fujimori T, Kawai-Yamada M, Yamaya T, Yanagisawa S, Uchimiya H (2009) Pleiotropic modulation of carbon and nitrogen metabolism in Arabidopsis plants overexpressing the NAD kinase2 gene. Plant Physiol 151:100–113
Takahashi H, Watanabe A, Tanaka A, Hashida S-n, Kawai-Yamada M, Sonoike K, Uchimiya H (2006) Chloroplast NAD kinase is essential for energy transduction through the xanthophyll cycle in photosynthesis. Plant Cell Physiol 47:1678–1682
Thordal-Christensen H, Zhang ZG, Wei YD, Collinge DB (2002) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194
Turner WL, Waller JC, Snedden WA (2005) Identification, molecular cloning and functional characterization of a novel NADH kinase from Arabidopsis thaliana (thale cress). Biochem J 385:217–223
Turner WL, Waller JC, Vanderbeld B, Snedden WA (2004) Cloning and characterization of two NAD kinases from Arabidopsis. Identification of a calmodulin binding isoform. Plant Physiol 135:1243–1255
Van Baarlen P, Van Belkum A, Summerbell RC, Crous PW, Thomma BP (2007) Molecular mechanisms of pathogenicity: how do pathogenic microorganisms develop cross-kingdom host jumps? FEMS Microbiol Rev 31:239–277
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66
Ziegler M (2000) New functions of a long-known molecule: emerging roles of NAD in cellular signaling. Chem Eur J 267:1550–1564
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This work was supported by KAKENHI Grant Numbers 19H04715 and 21H05647 to M. K-Y.
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MKY. and C. designed the study. C., YZ., AM., SNH, and MKY. performed the experiments. C., AM., TI., MY. and MKY. interpreted the data. C. and MKY. wrote the manuscript.
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Chaomurilege, Zu, Y., Miyagi, A. et al. Loss of chloroplast-localized NAD kinase causes ROS stress in Arabidopsis thaliana. J Plant Res 136, 97–106 (2023). https://doi.org/10.1007/s10265-022-01420-w
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DOI: https://doi.org/10.1007/s10265-022-01420-w