Skip to main content

Advertisement

Log in

Loss of chloroplast-localized NAD kinase causes ROS stress in Arabidopsis thaliana

  • Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

No new datasets were generated or analyzed in this study.

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

    Article  CAS  Google Scholar 

  • Apel K, Hier H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chassot C, Nawrath C, Métraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49:972–980

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 06:119–133

    Article  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hashida S-N, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot 103:819–824

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  CAS  Google Scholar 

  • Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425

    Article  CAS  Google Scholar 

  • Ohashi K, Kawai S, Koshimizu M, Murata K (2011) NADPH regulates human NAD kinase, a NADP+-biosynthetic enzyme. Mol Cell Biochem 355:57–64

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ziegler M (2000) New functions of a long-known molecule: emerging roles of NAD in cellular signaling. Chem Eur J 267:1550–1564

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by KAKENHI Grant Numbers 19H04715 and 21H05647 to M. K-Y.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Maki Kawai-Yamada.

Ethics declarations

Conflict of interest

No conflicts of interest declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 4549 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-022-01420-w

Keywords

Navigation