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Nitric Oxide as a Mediator of Cold Stress Response: A Transcriptional Point of View

Chapter

Abstract

Low temperature constitutes a major constraint for plant development and spreading and imprints plant biodiversity. Plant tolerance towards cold is a complex matter that relies on deep metabolic reprogramming principally governed by transcriptomic changes themselves controlled through multiple signalling pathways. A set of recent reports points out nitric oxide (NO) as a key element of signalling networks underlying plant response to low temperature. Based on the identification of several cold-regulated NO-dependent genes, that play key functions during plant response to temperature lowering, NO might sustain major functions during cold stress. This chapter summarizes our current knowledge on NO availability and bioactivity during low-temperature response, with a special emphasis on its implication in the regulation of gene expression.

Keywords

Antioxidants CBF genes Cold stress Nitrate reductase Osmoprotectant metabolism 

References

  1. Airaki M, Leterrier M, Mateos RM et al (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant, Cell Environ 35:281–295CrossRefGoogle Scholar
  2. Bai X, Chen J, Kong X et al (2012) Carbon monoxide enhances the chilling tolerance of recalcitrant Baccaurea ramiflora seeds via nitric oxide-mediated glutathione homeostasis. Free RadicBiol Med 53:710–720CrossRefGoogle Scholar
  3. Baudouin E (2011) The language of nitric oxide signalling. Plant Biol 13:233–242CrossRefPubMedGoogle Scholar
  4. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39CrossRefPubMedGoogle Scholar
  5. Besson-Bard A, Gravot A, Richaud P et al (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron up take. Plant Physiol 149:1302–1315CrossRefPubMedCentralPubMedGoogle Scholar
  6. Cantrel C, Vazquez T, Puyaubert J et al (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 189:415–427CrossRefPubMedGoogle Scholar
  7. Chaki M, Valderrama R, Fernández-Ocaña AM et al (2011) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813CrossRefPubMedCentralPubMedGoogle Scholar
  8. Chew YH, Halliday KJ (2011) A stress-free walk from Arabidopsis to crops. Curr Opin Biotechnol 22:281–286CrossRefPubMedGoogle Scholar
  9. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451CrossRefPubMedGoogle Scholar
  10. Corpas FJ, Chaki M, Fernández-Ocaña A et al (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722CrossRefPubMedGoogle Scholar
  11. Dutilleul C, Benhassaine-Kesri G, Demandre C et al (2012) Phytosphingosine-phosphate is a signal for AtMPK6 activation and Arabidopsis response to chilling. New Phytol 194:181–191CrossRefPubMedGoogle Scholar
  12. Esim N, Atici O, Mutlu S (2012) Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol Ind Health. doi: 10.1177/0748233712457444 Google Scholar
  13. Gaupels F, Kuruthukulangarakoola GT, Durner J (2011) Upstream and downstream signals of nitricoxide in pathogen defence. Curr Opin Plant Biol 14:707–714CrossRefPubMedGoogle Scholar
  14. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781CrossRefPubMedGoogle Scholar
  15. Guillas I, Guellim A, Rezé N et al (2012) Long chain base changes triggered by a short exposure of Arabidopsis to low temperature are altered by AHb1 non-symbiotic haemoglobin over expression. Plant Physiol Biochem 63:191–195CrossRefPubMedGoogle Scholar
  16. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1:e26CrossRefPubMedCentralPubMedGoogle Scholar
  17. Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751CrossRefPubMedGoogle Scholar
  18. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608CrossRefPubMedCentralPubMedGoogle Scholar
  19. Laxalt AM, Raho N, Have AT et al (2007) Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J BiolChem 282:21160–21168Google Scholar
  20. Lee B, Henderson DA, Zhu J-K (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175CrossRefPubMedCentralPubMedGoogle Scholar
  21. Leshem YY, Wills RBH, Ku VVV (1998) Evidence for the function of the free radical gas—nitricoxide (NO·)—as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833CrossRefGoogle Scholar
  22. Lindermayr C, Sell S, Müller B et al (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907CrossRefPubMedCentralPubMedGoogle Scholar
  23. Liu Y, Jiang H, Zhao Z, An L (2010) Nitric oxide synthase like activity-dependent nitric oxide production protects against chilling-induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant Physiol Biochem 48:936–944CrossRefPubMedGoogle Scholar
  24. Majláth I, Szalai G, Soós V et al (2012) Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. Physiol Plant 145:296–314CrossRefPubMedGoogle Scholar
  25. Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11CrossRefPubMedGoogle Scholar
  26. Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007CrossRefPubMedCentralPubMedGoogle Scholar
  27. Palmieri MC, Sell S, Huang X et al (2008) Nitricoxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186CrossRefPubMedGoogle Scholar
  28. Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232CrossRefGoogle Scholar
  29. Ruelland E, Vaultier MN, Zachowski A et al (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150CrossRefGoogle Scholar
  30. Serpa V, Vernal J, Lamattina L et al (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Biophys Res Commun 361:1048–1053CrossRefPubMedGoogle Scholar
  31. Shimoda Y, Nagata M, Suzuki A et al (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46:99–107CrossRefPubMedGoogle Scholar
  32. Singh SP, Singh Z, Swinny EE (2009) Postharvest nitric oxide fumigation delays fruit ripening and alleviates chilling injury during cold storage of Japanese plums (Prunus salicina Lindell). Postharvest Biol Technol 53:101–108CrossRefGoogle Scholar
  33. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97CrossRefPubMedGoogle Scholar
  34. Tada Y, Spoel SH, Pajerowska-Mukhtar K et al (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956CrossRefPubMedGoogle Scholar
  35. Tan J, Wang C, Xiang B et al (2013) Hydrogen peroxide and nitric oxide mediated cold- and dehydration-inducedmyo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant, Cell Environ 36:288–299CrossRefGoogle Scholar
  36. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105CrossRefPubMedGoogle Scholar
  37. Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577CrossRefPubMedCentralPubMedGoogle Scholar
  38. Usadel B, Bläsing OE, Gibon Y et al (2008) Multi level genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant, Cell Environ 31:518–547CrossRefGoogle Scholar
  39. Vogel JT, Zarka DG, Van Buskirk HA et al (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211CrossRefPubMedGoogle Scholar
  40. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant, Cell Environ 31:622–631CrossRefGoogle Scholar
  41. Xu M, Dong J, Zhang M et al (2012) Cold-induced endogenous nitric oxide generation plays a role in chilling tolerance of loquat fruit during postharvest storage. Postharvest Biol Technol 65:5–12CrossRefGoogle Scholar
  42. Yemets AI, Krasylenko YA, Lytvyn DI et al (2011) Nitric oxide signalling via cytoskeleton in plants. Plant Sci 181:545–554CrossRefPubMedGoogle Scholar
  43. Zaharah SS, Singh Z (2011) Post harvest nitric oxide fumigation alleviates chilling injury, delays fruit ripening and maintains quality in cold-stored “Kensington Pride” mango. Postharvest Biol Technol 60:202–210CrossRefGoogle Scholar
  44. Zhang LP, Mehta SK, Liu ZP et al (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419CrossRefPubMedGoogle Scholar
  45. Zhao M-G, Chen L, Zhang L-L et al (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767CrossRefPubMedCentralPubMedGoogle Scholar
  46. Zhao R, Sheng J, Lv S et al (2011) Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biol Technol 62:121–126CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Sorbonne Universités, UPMC Univ Paris 06Institut de Biologie Paris-Seine (IBPS)ParisFrance
  2. 2.Biologie du DéveloppementCNRSParisFrance
  3. 3.AgroécologieAgroSupDijonFrance
  4. 4.ERL CNRS 6300DijonFrance

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