Advertisement

Redox Regulation of Cold Stress Response

  • Venura HerathEmail author
Chapter

Abstract

The world crop production needs to be increased by 50% in 2050 in order to fulfill the nutrient requirement of 10 billion people. This task is made even more difficult by the severe environment conditions experienced by crops due to global warming. Plant biologists and breeders are facing a great challenge in order to improve crop yields along with developing stress-tolerant crops. In order to bioengineer future crops, it is essential to identify stress response mechanisms found in crops as well as their relatives. Then, susceptible crops can be developed into tolerant crops by careful fine-tuning of these mechanisms. Among the abiotic stresses, cold stress is considered as one of the major stresses that significantly reduces the crop production. Cold stress induces a complex network of signaling pathways mediated by transcription factors, plant hormones, reactive oxygen species (ROS), and other primary and secondary messengers. ROS are generated as a result of aerobic metabolism in plants. Due to its unstable nature, these ROS can damage various cellular components. In order to avoid such damage, plants have developed various redox regulatory systems. Interestingly, ROS are purposefully produced to serve as messengers by plants when they are under cold stress. ROS are long known as cytotoxic molecules that damage the cellular metabolism. However, emerging evidence is highlighting the importance of these ROS in acquiring cold and other abiotic stress tolerance.

Keywords

Cold stress Oxidative stress Redox regulation 

Notes

Acknowledgment

This work was supported by the National Research Council of Sri Lanka (NRC/14/117) and International Science Foundation, Sweden (C/5267-1).

References

  1. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240.  https://doi.org/10.1093/jxb/ert375CrossRefPubMedGoogle Scholar
  2. Chakraborty A, Bhattacharjee S (2015) Differential competence of redox-regulatory mechanism under extremes of temperature determines growth performances and cross tolerance in two indica rice cultivars. J Plant Physiol 176:65–77.  https://doi.org/10.1016/j.jplph.2014.10.016CrossRefPubMedGoogle Scholar
  3. Cheng F, Lu J, Gao M et al (2016) Redox signaling and CBF-responsive pathway are involved in salicylic acid-improved photosynthesis and growth under chilling stress in watermelon. Front Plant Sci 7:1–16.  https://doi.org/10.3389/fpls.2016.01519CrossRefGoogle Scholar
  4. Chinnusamy V, Hasanuzzaman M, Guo Z et al (2017) Transgenic centipedegrass (Eremochloa ophiuroides [Munro] Hack.) overexpressing S-adenosylmethionine decarboxylase (SAMDC) gene for improved cold tolerance through involvement of H 2 O 2 and NO signaling. Front Plant Sci 8:1655.  https://doi.org/10.3389/fpls.2017.01655CrossRefGoogle Scholar
  5. Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8:e23681.  https://doi.org/10.4161/psb.23681CrossRefPubMedGoogle Scholar
  6. Dahal K, Vanlerberghe GC (2017) Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought. New Phytol 213:560–571.  https://doi.org/10.1111/nph.14169CrossRefPubMedGoogle Scholar
  7. Das P, Nutan KK, Singla-Pareek SL, Pareek A (2015) Oxidative environment and redox homeostasis in plants: dissecting out significant contribution of major cellular organelles. Front Environ Sci 2:1–11.  https://doi.org/10.3389/fenvs.2014.00070CrossRefGoogle Scholar
  8. del Río LA, Corpas FJ, López-Huertas E, Palma JM (2018) Plant superoxide dismutases: function under abiotic stress conditions. Antioxidants Antioxid Enzym High Plants:1–26.  https://doi.org/10.1007/978-3-319-75088-0_1Google Scholar
  9. Einset J, Winge P, Bones A (2007) ROS signaling pathways in chilling stress. Plant Signal Behav 2:365–367.  https://doi.org/10.4161/psb.2.5.4461CrossRefPubMedPubMedCentralGoogle Scholar
  10. Farooq M, Wahid A, Kobayashi N et al (2009a) Plant drought stress: effects, mechanisms and management. Sustain Agric 29:185–212.  https://doi.org/10.1051/agroCrossRefGoogle Scholar
  11. Farooq M, Wahid A, Lee D-J et al (2009b) Advances in drought resistance of rice. CRC Crit Rev Plant Sci 28:199–217.  https://doi.org/10.1080/07352680902952173CrossRefGoogle Scholar
  12. Fiorani F (2005) The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 139:1795–1805.  https://doi.org/10.1104/pp.105.070789CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gaber A, Yoshimura K, Yamamoto T et al (2006) Glutathione peroxidase-like protein of Synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis. Physiol Plant 128:251–262.  https://doi.org/10.1111/j.1399-3054.2006.00730.xCrossRefGoogle Scholar
  14. Garretón V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526.  https://doi.org/10.1104/pp.009886CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gechev TS, Van Breusegem F, Stone JM et al (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101.  https://doi.org/10.1002/bies.20493CrossRefPubMedGoogle Scholar
  16. Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol 103:1067–1073.  https://doi.org/10.1104/pp.103.4.1067CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gupta DK, Palma JM, Corpas FJ (2018) Antioxidants and antioxidant enzymes in higher plants. Springer.Google Scholar
  18. Hasanuzzaman M, Nahar K, Alam MM et al (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684.  https://doi.org/10.3390/ijms14059643CrossRefPubMedPubMedCentralGoogle Scholar
  19. Heidarvand L, Maali Amiri R (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32:419–431.  https://doi.org/10.1007/s11738-009-0451-8CrossRefGoogle Scholar
  20. Herath V (2011) Transcriptional regulatory networks involved in plant responses to low temperature. The University of Maine, Orono.Google Scholar
  21. Hetherington SE, He J, Smillie RM (1989) Photoinhibition at low temperature in chilling-sensitive and -resistant plants. Plant Physiol 90:1609–1615.  https://doi.org/10.1104/pp.90.4.1609CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hossain MA, Bhattacharjee S, Armin S-M et al (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:1–19.  https://doi.org/10.3389/fpls.2015.00420CrossRefGoogle Scholar
  23. Hu WH, Song XS, Shi K et al (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581–588.  https://doi.org/10.1007/s11099-008-0098-5CrossRefGoogle Scholar
  24. Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation - what is important for metabolic adjustment? Plant Biol 12:395–405.  https://doi.org/10.1111/j.1438-8677.2009.00299.xCrossRefPubMedPubMedCentralGoogle Scholar
  25. Jha UC, Bohra A, Jha R (2017) Breeding approaches and genomics technologies to increase crop yield under low-temperature stress. Plant Cell Rep 36:1–35.  https://doi.org/10.1007/s00299-016-2073-0CrossRefPubMedGoogle Scholar
  26. Jiang Y, Peng D, Bai L-P et al (2013) Molecular switch for cold acclimation — anatomy of the cold-inducible promoter in plants. Biochemist 78:342–354.  https://doi.org/10.1134/S0006297913040032CrossRefGoogle Scholar
  27. Kundu P, Gill R, Ahlawat S et al (2018) Targeting the redox regulatory mechanisms for abiotic stress tolerance in crops. In Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants, pp. 151–220.CrossRefGoogle Scholar
  28. Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photoprotection. Photosynth Res 88:119–132.  https://doi.org/10.1007/s11120-006-9043-2CrossRefPubMedGoogle Scholar
  29. Lynch DV, Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter Rye seedlings (Secale cereale L. cv Puma). Plant Physiol 83:761–767.  https://doi.org/10.1104/pp.83.4.761CrossRefPubMedPubMedCentralGoogle Scholar
  30. Matsumura T, Tabayashi N, Kamagata Y et al (2002) Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol Plant 116:317–327.  https://doi.org/10.1034/j.1399-3054.2002.1160306.xCrossRefGoogle Scholar
  31. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci 96:8271–8276.  https://doi.org/10.1073/pnas.96.14.8271CrossRefPubMedGoogle Scholar
  32. Mühlenbock P, Szechynska-Hebda M, Plaszczyca M et al (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356.  https://doi.org/10.1105/tpc.108.059618CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170.  https://doi.org/10.3389/fpls.2014.00170CrossRefPubMedPubMedCentralGoogle Scholar
  34. Papagiannaki K, Lagouvardos K, Kotroni V, Papagiannakis G (2014) Agricultural losses related to frost events: use of the 850 hPa level temperature as an explanatory variable of the damage cost. Nat Hazards Earth Syst Sci 14:2375–2381.  https://doi.org/10.5194/nhess-14-2375-2014CrossRefGoogle Scholar
  35. Park M-R, Yun K-Y, Mohanty B et al (2010) Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ 33:2209–2230.  https://doi.org/10.1111/j.1365-3040.2010.02221.xCrossRefPubMedGoogle Scholar
  36. Park S, Lee C-M, Doherty CJ et al (2015) Regulation of the Arabidopsis CBF regulon by a complex low temperature regulatory network. Plant J 82:193.  https://doi.org/10.1111/tpj.12796CrossRefPubMedGoogle Scholar
  37. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69.  https://doi.org/10.3389/fpls.2015.00069CrossRefPubMedPubMedCentralGoogle Scholar
  38. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide--a central hub for information flow in plant cells. AoB Plants 2012:pls014.  https://doi.org/10.1093/aobpla/pls014CrossRefPubMedPubMedCentralGoogle Scholar
  39. Polidoros AN, Mylona PV, Pasentsis K et al (2005) The maize alternative oxidase 1a (Aox1a) gene is regulated by signals related to oxidative stress. Redox Rep 10:71–78.  https://doi.org/10.1179/135100005X21688CrossRefPubMedGoogle Scholar
  40. Poynton RA, Hampton MB (2014) Peroxiredoxins as biomarkers of oxidative stress. Biochim Biophys Acta - Gen Subj 1840:906–912.  https://doi.org/10.1016/j.bbagen.2013.08.001CrossRefGoogle Scholar
  41. Puhakainen T, Hess MW, Mäkelä P et al (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753.  https://doi.org/10.1023/B:PLAN.0000040903.66496.a4CrossRefPubMedGoogle Scholar
  42. Roxas VP, Smith RK, Smith RK, Allen RD (1997) Overexpression of glutathione s-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991.  https://doi.org/10.1038/nbt1097-988CrossRefPubMedGoogle Scholar
  43. Sahoo KK, Tripathi AK, Pareek A, Singla-Pareek SL (2013) Taming drought stress in rice through genetic engineering of transcription factors and protein kinases. Plant Stress 7(1):60–72.Google Scholar
  44. Saika H, Ohtsu K, Hamanaka S et al (2002) AOX1c, a novel rice gene for alternative oxidase; comparison with rice AOX1a and AOX1b. Genes Genet Syst 77:31–38.  https://doi.org/10.1266/ggs.77.31CrossRefPubMedGoogle Scholar
  45. Sato Y, Masuta Y, Saito K et al (2011) Enhanced chilling tolerance at the booting stage in rice by transgenic overexpression of the ascorbate peroxidase gene, OsAPXa. Plant Cell Rep 30:399–406.  https://doi.org/10.1007/s00299-010-0985-7CrossRefPubMedGoogle Scholar
  46. Sevilla F, Camejo D, Ortiz-Espín A et al (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66:2945–2955.  https://doi.org/10.1093/jxb/erv146CrossRefPubMedGoogle Scholar
  47. Shao HB, Chu LY, Zhao CX et al (2006) Plant gene regulatory network system under abiotic stress. Acta Biol Szeged 50:1–9Google Scholar
  48. Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Mol Plant 6:250–260.  https://doi.org/10.1093/mp/sss147CrossRefPubMedGoogle Scholar
  49. Shi Y, Ding Y, Yang S (2015) Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol 56:7–15.  https://doi.org/10.1093/pcp/pcu115CrossRefPubMedGoogle Scholar
  50. Sies H, Berndt C, Jones DP (2017) Oxidative stress. Annu Rev Biochem 86:715–748.  https://doi.org/10.1146/annurev-biochem-061516-045037CrossRefPubMedGoogle Scholar
  51. Souza LA, Monteiro CC, Carvalho RF et al (2017) Dealing with abiotic stresses: an integrative view of how phytohormones control abiotic stress-induced oxidative stress. Theor Exp Plant Physiol 29:109–127.  https://doi.org/10.1007/s40626-017-0088-8CrossRefGoogle Scholar
  52. Srougi MC, Miller HB, Witherow DS, Carson S (2013) Assessment of a novel group-centered testing schema in an upper-level undergraduate molecular biotechnology course. Biochem Mol Biol Educ 41:232–241.  https://doi.org/10.1002/bmb.20701CrossRefPubMedGoogle Scholar
  53. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270.  https://doi.org/10.1111/j.1365-3040.2011.02336.xCrossRefPubMedGoogle Scholar
  54. Teige M, Scheikl E, Eulgem T et al (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152.  https://doi.org/10.1016/j.molcel.2004.06.023CrossRefGoogle Scholar
  55. Turan Ö, Ekmekçi Y (2011) Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures. Acta Physiol Plant 33:67–78.  https://doi.org/10.1007/s11738-010-0517-7CrossRefGoogle Scholar
  56. Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9.  https://doi.org/10.1016/j.envexpbot.2009.05.008CrossRefGoogle Scholar
  57. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124.  https://doi.org/10.1038/nrm2330CrossRefPubMedPubMedCentralGoogle Scholar
  58. Vendruscolo ECG, Schuster I, Pileggi M et al (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376.  https://doi.org/10.1016/j.jplph.2007.05.001CrossRefPubMedGoogle Scholar
  59. Vitasse Y, Rebetez M (2018) Unprecedented risk of spring frost damage in Switzerland and Germany in 2017. Clim Chang 149:233–246.  https://doi.org/10.1007/s10584-018-2234-yCrossRefGoogle Scholar
  60. Wang Y, Wisniewski M, Meilan R et al (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. J Am Soc Hortic Sci 130:167–173Google Scholar
  61. Welti R, Li W, Li M et al (2002) Profiling membrane lipids in plant stress responses: role of phospholipase Dα in freezing-induced lipid changes in arabidopsis. J Biol Chem 277:31994–32002.  https://doi.org/10.1074/jbc.M205375200CrossRefPubMedGoogle Scholar
  62. Willems P, Mhamdi A, Simon S et al (2016) The ROS wheel: refining ROS transcriptional footprints in Arabidopsis. Plant Physiol 171(2016):1720.  https://doi.org/10.1104/pp.16.00420CrossRefPubMedPubMedCentralGoogle Scholar
  63. Xu J, Yang J, Duan X et al (2014) Increased expression of native cytosolic Cu/Zn superoxide dismutase and ascorbate peroxidase improves tolerance to oxidative and chilling stresses in cassava (Manihot esculenta Crantz). BMC Plant Biol 14:208.  https://doi.org/10.1186/s12870-014-0208-4CrossRefPubMedPubMedCentralGoogle Scholar
  64. Yamamoto M, Nasrallah JB (2013) In planta assessment of the role of thioredoxin h proteins in the regulation of S-locus receptor kinase signaling in transgenic Arabidopsis. Plant Physiol 163:1387–1395.  https://doi.org/10.1104/pp.113.225672CrossRefPubMedPubMedCentralGoogle Scholar
  65. Yang MT, Chen SL, Lin CY, Chen YM (2005) Chilling stress suppresses chloroplast development and nuclear gene expression in leaves of mung bean seedlings. Planta 221:374–385.  https://doi.org/10.1007/s00425-004-1451-yCrossRefPubMedGoogle Scholar
  66. Yun K-Y, Park MR, Mohanty B et al (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol 10:16.  https://doi.org/10.1186/1471-2229-10-16CrossRefPubMedPubMedCentralGoogle Scholar
  67. Zandalinas SI, Mittler R, Balfagón D et al (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12.  https://doi.org/10.1111/ppl.12540CrossRefPubMedGoogle Scholar
  68. Zhang L, Li Z, Li J, Wang A (2013) Ectopic overexpression of SsCBF1, a CRT/DRE-binding factor from the nightshade plant Solanum lycopersicoides, confers freezing and salt tolerance in transgenic Arabidopsis. PLoS One 8:15–17.  https://doi.org/10.1371/journal.pone.0061810CrossRefGoogle Scholar
  69. Zhang M, Su J, Zhang Y et al (2018) Conveying endogenous and exogenous signals: MAPK cascades in plant growth and defense. Curr Opin Plant Biol 45:1–10.  https://doi.org/10.1016/j.pbi.2018.04.012CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Agricultural Biology, Faculty of AgricultureUniversity of PeradeniyaPeradeniyaSri Lanka

Personalised recommendations