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Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis


Autoři: Yechun Hong aff001;  Zhen Wang aff001;  Huazhong Shi aff003;  Juanjuan Yao aff001;  Xue Liu aff001;  Fuxing Wang aff001;  Liang Zeng aff001;  Zhi Xie aff001;  Jian-Kang Zhu aff001
Působiště autorů: Shanghai Center for Plant Stress Biology and Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China aff001;  University of Chinese Academy of Sciences, Shanghai, P.R. China aff002;  Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, Texas, United States of America aff003;  Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana, United States of America aff004
Vyšlo v časopise: Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis. PLoS Genet 16(6): e1008892. doi:10.1371/journal.pgen.1008892
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008892

Souhrn

Nicotinamide adenine dinucleotide (NAD) is an essential coenzyme that has emerged as a central hub linking redox equilibrium and signal transduction in living organisms. The homeostasis of NAD is required for plant growth, development, and adaption to environmental cues. In this study, we isolated a chilling hypersensitive Arabidopsis thaliana mutant named qs-2 and identified the causal mutation in the gene encoding quinolinate synthase (QS) critical for NAD biosynthesis. The qs-2 mutant is also hypersensitive to salt stress and abscisic acid (ABA) but resistant to drought stress. The qs-2 mutant accumulates a reduced level of NAD and over-accumulates reactive oxygen species (ROS). The ABA-hypersensitivity of qs-2 can be rescued by supplementation of NAD precursors and by mutations in the ABA signaling components SnRK2s or RBOHF. Furthermore, ABA-induced over-accumulation of ROS in the qs-2 mutant is dependent on the SnRK2s and RBOHF. The expression of QS gene is repressed directly by ABI4, a transcription factor in the ABA response pathway. Together, our findings reveal an unexpected interplay between NAD biosynthesis and ABA and stress signaling, which is critical for our understanding of the regulation of plant growth and stress responses.

Klíčová slova:

Arabidopsis thaliana – Biosynthesis – Leaves – Phenotypes – Plant growth and development – Plant resistance to abiotic stress – Redox signaling – Seedlings


Zdroje

1. Wang P, Zhao Y, Li Z, Hsu CC, Liu X, et al. (2018) Reciprocal Regulation of the TOR Kinase and ABA Receptor Balances Plant Growth and Stress Response. Mol Cell 69: 100–112.e106. doi: 10.1016/j.molcel.2017.12.002 29290610

2. Miao CB, Wang Z, Zhang L, Yao JJ, Hua K, et al. (2019) The grain yield modulator miR156 regulates seed dormancy through the gibberellin pathway in rice. Nature Communications 10.

3. Bockwoldt M, Houry D, Niere M, Gossmann TI, Reinartz I, et al. (2019) Identification of evolutionary and kinetic drivers of NAD-dependent signaling. Proceedings of the National Academy of Sciences of the United States of America 116: 15957–15966. doi: 10.1073/pnas.1902346116 31341085

4. Hashida SN, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Annals of Botany 103: 819–824. doi: 10.1093/aob/mcp019 19201765

5. Gakiere B, Hao JF, de Bont L, Petriacq P, Nunes-Nesi A, et al. (2018) NAD(+) Biosynthesis and Signaling in Plants. Critical Reviews in Plant Sciences 37: 259–307.

6. Zhu JK (2016) Abiotic Stress Signaling and Responses in Plants. Cell 167: 313–324. doi: 10.1016/j.cell.2016.08.029 27716505

7. Koornneef M, Leon-Kloosterziel KM, Schwartz SH, Zeevaart JAD (1998) The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiology and Biochemistry 36: 83–89.

8. Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends in Plant Science 4: 472–478. doi: 10.1016/s1360-1385(99)01497-1 10562731

9. Toh S, Imamura A, Okamoto M, Nakabayashi K, Kamiya Y, et al. (2005) Regulation of ABA levels in Arabidopsis seeds by high temperature: Contribution of NCED genes. Plant and Cell Physiology 46: S81–S81.

10. Lefebvre V, North H, Frey A, Sotta B, Seo M, et al. (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant Journal 45: 309–319. doi: 10.1111/j.1365-313X.2005.02622.x 16412079

11. Schwartz SH, LeonKloosterziel KM, Koornneef M, Zeevaart JAD (1997) Biochemical characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiology 114: 161–166. doi: 10.1104/pp.114.1.161 9159947

12. Nambara E, Kawaide H, Kamiya Y, Naito S (1998) Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant and Cell Physiology 39: 853–858. doi: 10.1093/oxfordjournals.pcp.a029444 9787459

13. Yoshida T, Obata T, Feil R, Lunn JE, Fujita Y, et al. (2019) The Role of Abscisic Acid Signaling in Maintaining the Metabolic Balance Required for Arabidopsis Growth under Nonstress Conditions. Plant Cell 31: 84–105. doi: 10.1105/tpc.18.00766 30606780

14. Klingler JP, Batelli G, Zhu JK (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. Journal of Experimental Botany 61: 3199–3210. doi: 10.1093/jxb/erq151 20522527

15. Finkelstein R, Gampala SSL, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Molecular Biology 59: 253–267. doi: 10.1007/s11103-005-8767-2 16247556

16. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, et al. (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant Journal 61: 672–685. doi: 10.1111/j.1365-313X.2009.04092.x 19947981

17. Huang XZ, Zhang XY, Gong ZZ, Yang SH, Shi YT (2017) ABI4 represses the expression of type-A ARRs to inhibit seed germination in Arabidopsis. Plant Journal 89: 354–365. doi: 10.1111/tpj.13389 27711992

18. Cho D, Shin DJ, Jeon BW, Kwak JM (2009) ROS-Mediated ABA Signaling. Journal of Plant Biology 52: 102–113.

19. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, et al. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734. doi: 10.1038/35021067 10963598

20. Considine MJ, Foyer CH (2014) Redox Regulation of Plant Development. Antioxidants & Redox Signaling 21: 1305–1326.

21. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, et al. (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. Febs Letters 583: 2982–2986. doi: 10.1016/j.febslet.2009.08.033 19716822

22. Bartoli CG, Casalongue CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany 94: 73–88.

23. Bethke PC, Libourel IGL, Aoyama N, Chung YY, Still DW, et al. (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiology 143: 1173–1188. doi: 10.1104/pp.106.093435 17220360

24. Sarath G, Hou GC, Baird LM, Mitchell RB (2007) Reactive oxygen species, ABA and nitric oxide interactions on the germination of warm-season C-4-grasses. Planta 226: 697–708. doi: 10.1007/s00425-007-0517-z 17431667

25. Meinhard M, Grill E (2001) Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. Febs Letters 508: 443–446. doi: 10.1016/s0014-5793(01)03106-4 11728469

26. Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of AB12 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214: 775–782. doi: 10.1007/s00425-001-0675-3 11882947

27. Hua DP, Wang C, He JN, Liao H, Duan Y, et al. (2012) A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis. Plant Cell 24: 2546–2561. doi: 10.1105/tpc.112.100107 22730405

28. Arend M, Schnitzler JP, Ehlting B, Hansch R, Lange T, et al. (2009) Expression of the Arabidopsis Mutant abi1 Gene Alters Abscisic Acid Sensitivity, Stomatal Development, and Growth Morphology in Gray Poplars. Plant Physiology 151: 2110–2119. doi: 10.1104/pp.109.144956 19837818

29. Noctor G, Foyer CH (2016) Intracellular Redox Compartmentation and ROS-Related Communication in Regulation and Signaling. Plant Physiol 171: 1581–1592. doi: 10.1104/pp.16.00346 27208308

30. Lin SJ, Defossez PA, Guarente L (2000) Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289: 2126–2128. doi: 10.1126/science.289.5487.2126 11000115

31. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9: 490–498. doi: 10.1016/j.tplants.2004.08.009 15465684

32. Noctor G, Queval G, Gakiere B (2006) NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. Journal of Experimental Botany 57: 1603–1620. doi: 10.1093/jxb/erj202 16714307

33. Katoh A, Uenohara K, Akita M, Hashimoto T (2006) Early steps in the biosynthesis of NAD in Arabidopsis start with aspartate and occur in the plastid. Plant Physiology 141: 851–857. doi: 10.1104/pp.106.081091 16698895

34. Sakuraba H, Tsuge H, Yoneda K, Katunuma N, Ohshima T (2005) Crystal structure of the NAD biosynthetic enzyme quinolinate synthase. Journal of Biological Chemistry 280: 26645–26648. doi: 10.1074/jbc.C500192200 15937336

35. Hunt L, Holdsworth MJ, Gray JE (2007) Nicotinamidase activity is important for germination. Plant Journal 51: 341–351. doi: 10.1111/j.1365-313X.2007.03151.x 17587307

36. Wang GD, Pichersky E (2007) Nicotinamidase participates in the salvage pathway of NAD biosynthesis in Arabidopsis. Plant Journal 49: 1020–1029. doi: 10.1111/j.1365-313X.2006.03013.x 17335512

37. Li W, Zhang FX, Chang YW, Zhao T, Schranz ME, et al. (2015) Nicotinate O-Glucosylation Is an Evolutionarily Metabolic Trait Important for Seed Germination under Stress Conditions in Arabidopsis thaliana. Plant Cell 27: 1907–1924. doi: 10.1105/tpc.15.00223 26116607

38. Amor Y, Babiychuk E, Inze D, Levine A (1998) The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. Febs Letters 440: 1–7. doi: 10.1016/s0014-5793(98)01408-2 9862413

39. Taniguchi M, Kobe A, Kato M, Sugiyama T (1995) Aspartate-Aminotransferase Isozymes in Panicum-Miliaceum L, an Nad-Malic Enzyme-Type C-4 Plant—Comparison of Enzymatic-Properties, Primary Structures, and Expression Patterns. Archives of Biochemistry and Biophysics 318: 295–306. doi: 10.1006/abbi.1995.1233 7733657

40. Wu RR, Zhang FX, Liu LY, Li W, Pichersky E, et al. (2018) MeNA, Controlled by Reversible Methylation of Nicotinate, Is an NAD Precursor that Undergoes Long-Distance Transport in Arabidopsis. Molecular Plant 11: 1264–1277. doi: 10.1016/j.molp.2018.07.003 30055263

41. Schippers JHM, Nunes-Nesi A, Apetrei R, Hille J, Fernie AR, et al. (2008) The Arabidopsis onset of leaf death5 Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing. Plant Cell 20: 2909–2925. doi: 10.1105/tpc.107.056341 18978034

42. Wei M, Zhuang Y, Li H, Li P, Huo H, et al. (2019) The cloning and characterization of hypersensitive to salt stress mutant, affected in quinolinate synthase, highlights the involvement of NAD in stress-induced accumulation of ABA and proline. Plant J.

43. Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31: 629–638. doi: 10.1046/j.1365-313x.2002.01384.x 12207652

44. Qi YP, Tsuda K, Nguyen LV, Wang X, Lin JS, et al. (2011) Physical Association of Arabidopsis Hypersensitive Induced Reaction Proteins (HIRs) with the Immune Receptor RPS2. Journal of Biological Chemistry 286: 31297–31307. doi: 10.1074/jbc.M110.211615 21757708

45. Hashida SN, Itami T, Takahashi H, Takahara K, Nagano M, et al. (2010) Nicotinate/nicotinamide mononucleotide adenyltransferase-mediated regulation of NAD biosynthesis protects guard cells from reactive oxygen species in ABA-mediated stomatal movement in Arabidopsis. J Exp Bot 61: 3813–3825. doi: 10.1093/jxb/erq190 20591898

46. Noctor G, Mhamdi A, Foyer CH (2014) The Roles of Reactive Oxygen Metabolism in Drought: Not So Cut and Dried. Plant Physiology 164: 1636–1648. doi: 10.1104/pp.113.233478 24715539

47. Zhan XQ, Qian BL, Cao FQ, Wu WW, Yang L, et al. (2015) An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses. Nature Communications 6.

48. Wang Z, Wang FX, Hong YC, Huang JR, Shi HZ, et al. (2016) Two Chloroplast Proteins Suppress Drought Resistance by Affecting ROS Production in Guard Cells. Plant Physiology 172: 2491–2503. doi: 10.1104/pp.16.00889 27744298

49. Hong Y, Wang Z, Liu X, Yao J, Kong X, et al. (2020) Two Chloroplast Proteins Negatively Regulate Plant Drought Resistance Through Separate Pathways. Plant Physiol 182: 1007–1021. doi: 10.1104/pp.19.01106 31776182

50. Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell and Environment 39: 1140–1160.

51. Chini CCS, Tarrago MG, Chini EN (2017) NAD and the aging process: Role in life, death and everything in between. Molecular and Cellular Endocrinology 455: 62–74. doi: 10.1016/j.mce.2016.11.003 27825999

52. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci U S A 106: 8380–8385. doi: 10.1073/pnas.0903144106 19420218

53. Kulik A, Wawer I, Krzywinska E, Bucholc M, Dobrowolska G (2011) SnRK2 Protein Kinases-Key Regulators of Plant Response to Abiotic Stresses. Omics-a Journal of Integrative Biology 15: 859–872. doi: 10.1089/omi.2011.0091 22136638

54. Hashida S, Itami T, Takahara K, Hirabayashi T, Uchimiya H, et al. (2016) Increased Rate of NAD Metabolism Shortens Plant Longevity by Accelerating Developmental Senescence in Arabidopsis. Plant and Cell Physiology 57: 2427–2439. doi: 10.1093/pcp/pcw155 27590711

55. Li W, Zhang FX, Wu RR, Jia LJ, Li GS, et al. (2017) A Novel N-Methyltransferase in Arabidopsis Appears to Feed a Conserved Pathway for Nicotinate Detoxification among Land Plants and Is Associated with Lignin Biosynthesis. Plant Physiology 174: 1492–1504. doi: 10.1104/pp.17.00259 28533213

56. Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13: 2063–2083. doi: 10.1105/tpc.010101 11549764

57. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. doi: 10.1046/j.1365-313x.1998.00343.x 10069079

58. Wang Z, Wang FX, Hong YC, Yao JJ, Ren ZZ, et al. (2018) The Flowering Repressor SVP Confers Drought Resistance in Arabidopsis by Regulating Abscisic Acid Catabolism. Molecular Plant 11: 1184–1197.

59. Vilcheze C, Weisbrod TR, Chen B, Kremer L, Hazbon MH, et al. (2005) Altered NADH/NAD(+) ratio mediates coresistance to isoniazid and ethionamide in mycobacteria. Antimicrobial Agents and Chemotherapy 49: 708–720. doi: 10.1128/AAC.49.2.708-720.2005 15673755

60. Ren ZZ, Wang Z, Zhou XE, Shi HZ, Hong YC, et al. (2017) Structure determination and activity manipulation of the turfgrass ABA receptor FePYR1. Scientific Reports 7.

61. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, et al. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30: 325–327. doi: 10.1093/nar/30.1.325 11752327

62. Saleh A, Alvarez-Venegas R, Avramova Z (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nature Protocols 3: 1018–1025. doi: 10.1038/nprot.2008.66 18536649


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