Unlocking the mystery of plants’ survival capability under waterlogging stress

Authors

  • Kazi Khayrul Bashar Basic and Applied Research on Jute Project, Bangladesh Jute Research Institute, Manik Mia Avenue, Dhaka 1207, Bangladesh
  • Md. Zablul Tareq Basic and Applied Research on Jute Project, Bangladesh Jute Research Institute, Manik Mia Avenue, Dhaka 1207, Bangladesh
  • Md. Shahidul Islam Basic and Applied Research on Jute Project, Bangladesh Jute Research Institute, Manik Mia Avenue, Dhaka 1207, Bangladesh

DOI:

https://doi.org/10.14719/pst.2020.7.2.663

Keywords:

Waterlogging, crop plants, physiological pathways, survival mechanism, signaling

Abstract

Waterlogging is a major abiotic stress affecting crop plants throughout the world, which hampers crop growth and causes yield loss. There are various types of responses in plants under this stress through the combined operation of different signaling and physiological pathways. However, the correlation between these pathways is extremely limited and not well described in the published papers. Therefore, the complex waterlogging stress-tolerance mechanisms need to be presented most coherently for a comprehensive understanding of this stress. Here, we present sequential responses in plants under oxygen-deprivation stress. The regulation of the N-end rule pathway may be treated as the initial signaling in plants after facing waterlogging stress, but still, it remains a controversial topic. All the pathways under waterlogging stress are directly or indirectly related to glycolysis, tricarboxylic acid (TCA) cycle, programmed cell death (PCD) and removal of reactive oxygen species (ROS). Scientists may consider alanine aminotransferase as the main controlling switch for surviving of plants under waterlogging stress. Triggering the genes responsible for alanine aminotransferase may act as a crucial one to develop a waterlogging tolerant plant due to its ability to control anaerobic fermentation, TCA cycle and efficient utilization of carbons.

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References

1. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 2011;11(163):1-14. https://doi.org/10.1186/1471-2229-11-163

2. Patel PK, Singh AK, Tripathi N, Yadav D, Hemantaranjan A. Flooding: Abiotic constraint limiting vegetable productivity. Adv Plants Agri Res 2014;1(3):96-103. https://doi.org/10.15406/apar.2014.01.00016

3. Rivera-Contreras, IK, Zamora-Hernández T, Huerta-Heredia AA, Capataz-Tafur J, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM. Transcriptomic analysis of submergence-tolerant and sensitive Brachypodium distachyon ecotypes reveals oxidative stress as a major tolerance factor. Sci Rep. 2016; 6:27686. https://doi.org/10.1038/srep27686

4. Sasidharan R, Voesenek LACJ. Ethylene-mediated acclimations to flooding Stress. Plant Physiol. 2015;169(1):3-12. https://doi.org/10.1104/pp.15.00387

5. Yang SF, Hoffman NE. Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol. 1984;35:155-89. https://doi.org/10.1146/annurev.pp.35.060184.001103

6. Jackson MB. Ethylene and responses of plants to soil waterlogging and submergence. Annu Rev Plant Biol. 1985;36(1):145-74. https://doi.org/10.1146/annurev.pp.36.060185.001045

7. Ju C, Van de Poel B, Cooper ED, James H, Thierer JH, Gibbons TR, Delwiche CF, Chang C. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat Plants. 2015; 1:14004. https://doi.org/10.1038/nplants.2014.4

8. Chen Y, Randlett MD, Findell JL, Schaller GE. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem. 2002;277(22):19861-66. https://doi.org/10.1074/jbc.M201286200

9. Grefen C, Stadele K, Ruzicka K, Obrdlik P, Harter K, Horak J. Subcellular localization and In Vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol Plant. 2008;1(2):308-20. https://doi.org/10.1093/mp/ssm015

10. Bisson MMA, Bleckmann A, Allekotte S, Groth G. EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem Journal. 2009;424(1):1-6. https://doi.org/10.1042/BJ20091102

11. Dong C, Rivarola M, Resnick JS, Maggin BD, Chang C. Subcellular co-localization of Arabidopsis RTE1 and ETR1 supports a regulatory role for RTE1 in ETR1 ethylene signaling. Plant J. 2008;53(2):275-86. https://doi.org/10.1111/j.1365-313X.2007.03339.x

12. Xie C, Zhangy J, Zhouy H, Li J, Zhang Z, Wang D, Chen S. Serine/threonine kinase activity in the putative histidine kinase-like ethylene receptor NTHK1 from tobacco. Plant J. 2003;33(2):385-93. https://doi.org/10.1046/j.1365-313X.2003.01631.x

13. Ju C, Chang C. Advances in ethylene signaling: protein complexes at the endoplasmic reticulum membrane. AoB Plants 2012; pls031. https://doi.org/10.1093/aobpla/pls031

14. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P. EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F Box proteins: EBF1 and EBF2. Cell. 2003;115(6):679-89. https://doi.org/10.1016/S0092-8674(03)00968-1

15. Song L, Liu D. Ethylene and plant responses to phosphate deficiency. Front Plant Sci. 2015;6:796. https://doi.org/10.3389/fpls.2015.00796

16. Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, Van Dongen JT. Making sense of low oxygen sensing. Trends Plant Sci. 2012;17(3):129-38. https://doi.org/10.1016/j.tplants.2011.12.004

17. Nakano T, Suzuki K, Fujimura T, Shinshi H. Genome-wide analysis of the ERF gene family in Arabidopsis and Rice. Plant Physiol. 2006; 140(2):411-32. https://doi.org/10.1104/pp.105.073783

18. Wei X, Xu H, Rong W, Ye X, Zhang Z. Constitutive expression of a stabilized transcription factor ERFVII enhances waterlogging tolerance in wheat without penalizing grain yield. Plant Cell Environ. 2019; 42(5):1471-85. https://doi.org/10.1111/pce.13505

19. Yu F, Liang K, Fang T, Zhao H, Han X, Cai M, Qiu F. A group VII ethylene response factor gene, ZmEREB180, coordinates waterlogging tolerance in maize seedlings. Plant Biotechnol J. 2019; (Epub ahead of print). https://doi.org/10.1111/pbi.13140

20. Eysholdt-Derzso E, Sauter M. Hypoxia and the group VII ethylene response transcription factor HRE2 promote adventitious root elongation in Arabidopsis. Plant Biol. 2018; 1:103-08. http://dx.doi.org/10.1111/plb.12873

21. Giuntoli B, Perata P. Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles. Plant Physiol. 2018;176(2):1143-55. https://doi.org/10.1104/pp.17.01225

22. Gil-Monreal M, Giuntoli B, Zabalza A, Licausi F, Royuela M. 2019. ERF-VII transcription factors induce ethanol fermentation in response to amino acid biosynthesis-inhibiting herbicides. J Exp Bot. 2019;70(20):5839–51 https://doi.org/10.1093/jxb/erz355

23. Fan W, Yang Y, Wang Z, Yin Y, Yu C, Shi Q, Guo J, Xuan L, Hua J. Molecular cloning and expression analysis of three ThERF s involved in the response to waterlogging stress of Taxodium ‘Zhongshanshan406’, and subcellular localization of the gene products. PeerJ. 2018;12(6):e4434. http://dx.doi.org/10.7717/peerj.4434

24. Yin D, Sun D, Han Z, Ni D, Norri A, Jiang C. PhERF2, an ethylene-responsive element binding factor, plays an essential role in waterlogging tolerance of Petunia. Hort Res. 2019; 6(1):83. https://doi.org/10.1038/s41438-019-0165-z

25. Gibbs DJ, Tedds HM, Labandera A, Bailey M, White MD, Hartman S, Sprigg C, Mogg SL, Osborne R, Dambire C, Boeckx T, Paling Z, Voesenek LACJ, Flashman E, Holdsworth MJ. Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2. Nat Commun. 2018;9(1):5438. https://doi.org/10.1038/s41467-018-07875-7

26. Chen M, Zhu F, Wang F, Ye N, Gao B, Chen X, Zhao S, Fan T, Cao Y, Liu T, Su Z, Xie L, Hu Q, Wu H, Xiao S, Zhang J, Liu Y. Alternative splicing and translation play important roles in hypoxic germination in rice. J Exp Bot. 2018;70(3):817-33. https://doi.org/10.1093/jxb/ery393

27. Lin C, Chao Y, Chen W, Ho H, Chou M, Li Y, Wu Y, Yang H, Hsieh H, Lin C, Wu F, Chou S, Jen H, Huang Y, Irene D, Wu W, Wu J, Gibbs DJ, Ho M, Shih M. Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. PNAS. 2019;116(8):201818507. https://doi.org/10.1073/pnas.1818507116

28. Licausi F, M Kosmacz, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, Van Dongen JT. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature. 2011;479(7373):419-23. https://doi.org/10.1038/nature10536

29. Licausi F. Molecular elements of low-oxygen signaling in plants. Physiol. Plant. 2013;148(1):1-8. https://doi.org/10.1111/ppl.12011

30. Liao, Y, Jeng J, Wang C, Wang S, Chang S. Removal of N-terminal methionine from recombinant proteins by engineered E. coli methionine aminopeptidase. Protein Sci. 2004;13(7):1802-10. https://doi.org/10.1110/ps.04679104

31. Kwon YT, Kashina AS, Davydov IV, Hu R, An JY, Seo JW, Du F. A Varshavsky, An essential role of N-terminal arginylation in cardiovascular development. Science. 2002;297(5578):6-99. https://doi.org/10.1126/science.1069531

32. 32. Graciet E, Mesiti F, Wellmer F. Structure and evolutionary conservation of the plant N-end rule pathway. Plant J. 2010;61(5):741-51. https://doi.org/10.1111/j.1365-313X.2009.04099.x

33. Voges D, Zwickl P, Baumeister W. The 26S Proteasome: A molecular machine designed for controlled proteolysis. Annu Rev Biochem. 1999,68:1015-68. https://doi.org/10.1146/annurev.biochem.68.1.1015

34. Garzon M, Eifler K, Faust A, Scheel H, Hofmann K, Koncz C, Yephremov A, Bachmair A. PRT6/At5g02310 encodes an Arabidopsis ubiquitin ligase of the N-end rule pathway with arginine specificity and is not the CER3 locus. FEBS Lett. 2007; 581(17):3189-96. https://doi.org/10.1016/j.febslet.2007.06.005

35. Vallon U, Kull U. Localization of proteasomes in plant cells. Protoplasma. 1994;182(1-2):15-18. https://doi.org/10.1007/BF01403684

36. Kosmacz M, Parlanti S, Schwarzländer M, Kragler F, Licausi F, Van Dongen JT. The stability and nuclear localization of the transcription factor RAP2.12 are dynamically regulated by oxygen concentration. Plant Cell Environ. 2015;38(6):1094-03. https://doi.org/10.1111/pce.12493

37. Hartman S, Liu Z, van Veen H, Vicente J, Reinen E, Martopawiro S, et al. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat Commun. 2019; 10:4020. https://doi.org/10.1038/s41467-019-12045-4

38. Hess N, Klode M, Anders M, Sauter M. The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiol Plant. 2011;143(1):41-49. https://doi.org/10.1111/j.1399-3054.2011.01486.x

39. Tan X, Zwiazek JJ. Stable expression of aquaporins and hypoxia-responsive genes in adventitious roots are linked to maintaining hydraulic conductance in tobacco (Nicotiana tabacum) exposed to root hypoxia. PLOS One 2019; 14(2):e0212059. https://doi.org/10.1371/journal.pone.0212059

40. Paul MV, Iyer S, Amerhauser C, Lehmann M, Van Dongen JT, Geigenberger P. Oxygen sensing via the ethylene response transcription factor RAP2.12 affects plant metabolism and performance under both normoxia and hypoxia. Plant Physiol. 2016;172(1):141-53. https://doi.org/10.1104/pp.16.00460

41. Davies DD, Grego S, Kenworthy P. The control of the production of lactate and ethanol by higher Plants. Planta. 1974; 118(4):297-310. https://doi.org/10.1007/BF00385580

42. Roberts JKM, Hooks MA, Miaullis AP, Edwards S, Webster C. Contribution of malate and amino acid metabolism to cytoplasmic pH regulation in hypoxic maize root tips studied using nuclear magnetic resonance spectroscopy. Plant Physiol. 1992; 98(2):480-87. https://doi.org/10.1104/pp.98.2.480

43. Ricard B, Couée I, Raymond P, Saglio PH, Saint-Ges V, Pradet A. Plant metabolism under hypoxia and anoxia. Plant Physiol. Biochem. 1994; 32(1):1-10

44. Pan D, Wang G, Wang T, Jia Z, Guo Z, Zhang J. AdRAP2.3, a Novel Ethylene Response Factor VII from Actinidia deliciosa, Enhances Waterlogging Resistance in Transgenic Tobacco through Improving Expression Levels of PDC and ADH Genes. Int J Mol Sci. 2019;20(5):1189. https://doi.org/10.3390/ijms20051189

45. Xu B, Xie L, Cheng Y, Lu G, Zheng P, Zhang X. Cloning of Lactate dehydrogenase Gene and Effect on the Waterlogging Tolerance of Brassica napus L. Adv J Food Sci Tech. 2012;4(5):332-36

46. Das A, Uchimiya H. Oxygen stress and adaptation of a semi-aquatic plant: rice (Oryza sativa). J Plant Res. 2002;115(5):315-20. https://doi.org/10.1007/s10265-002-0043-9

47. Ren C, Kong C, Yan K, Zhang H, Luo Y, Xie Z. Elucidation of the molecular responses to waterlogging in Sesbania cannabina roots by transcriptome profling. Sci Rep. 2017;7:9256. https://doi.org/10.1038/s41598-017-07740-5

48. Parent C, Capelli N, Berger A, Crevecoeur M, Dat JF. An Overview of plant responses to soil waterlogging. Plant Stress. 2008; 2:20-27

49. Xia J, Saglio PH. Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiol. 1992; 100(1):40-46. https://doi.org/10.1104/pp.100.1.40

50. Wiebold WJ. Crop plant responses to flooding. Insect pest & crop management newsletter, University of Missouri. https://ipm.missouri.edu/IPCM/2015/6/Crop-Plant-Response-to-Flooding/ (accessed 10 November 2019). 2015; 25:6-7

51. Gout E, Boisson A, Aubert S, Douce R, Bligny R. Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. carbon-13 and phosphorous-31 nuclear magnetic resonance studies. Plant Physiol. 2001;125(2):912-25. https://doi.org/10.1104/pp.125.2.912

52. Ferreira de Sousa, FA, Sodek L. The metabolic response of plants to oxygen deficiency. Braz J Plant Physiol. 2002; 14(2):83-94. http://dx.doi.org/10.1590/S1677-04202002000200002

53. Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, et al. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol. 2010; 152(3):1501-13. https://doi.org/10.1104/pp.109.150045

54. Maricle BR, White SJ, Meraz A, Maforo NG, Biggs TN, Martin NM, et al. Effect of ethanol toxicity on enzyme activity in anaerobic respiration in plants. Trans Kans Acad Sci. 2014; 117(3-4):237-44. https://doi.org/10.1660/062.117.0309

55. Arcara PG, Ronchi VN. Effect of ethyl alcohol on the mitotic cycle of Allium cepa root meristems. Caryologia. 1967; 20(3):229-32. https://doi.org/10.1080/00087114.1967.10796261

56. Perata P, Alpi A, Loschiavo F. Influence of ethanol on plant cells and tissues. J. Plant Physiol. 1986; 126(2-3):181-88. https://doi.org/10.1016/S0176-1617(86)80019-0

57. Dordas C, Rivoal J, Hill RD. Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot. 2003;91(2):173-178. https://doi.org/10.1093/aob/mcf115

58. Voesenek LACJ, Sasidharan R, Visser EJW, Bailey-Serres J. Flooding stress signaling through perturbations in oxygen, ethylene, nitric oxide and light. New Phytol. 2016;209(1):39-43. https://doi.org/10.1111/nph.13775

59. Bai X, Long J, He X, Yan J, Chen X, Tan Y, Li K, Chen L, Xu H. Overexpression of spinach non-symbiotic hemoglobin in Arabidopsis resulted in decreased NO content and lowered nitrate and other abiotic stresses tolerance. Sci Rep. 2016; 6:26400. https://doi.org/10.1038/srep26400

60. Du H, Shen X, Huang Y, Huang M, Zhang Z. Overexpression of Vitreoscilla hemoglobin increases waterlogging tolerance in Arabidopsis and maize. BMC Plant Biol. 2016;16(1):35. https://doi.org/10.1186/s12870-016-0728-1

61. Li X, Peng R, Fan H, Xiong A, Yao Q, Cheng Z, Li Y. Vitreoscilla hemoglobin overexpression increases submergence tolerance in cabbage. Plant Cell Rep. 2005;23(10-11):710-15. https://doi.org/10.1007/s00299-004-0872-1

62. Sairam RK, Kumutha D, Ezhilmathi K. Waterlogging tolerance: nonsymbiotic hemoglobin-nitric oxide homeostasis and antioxidants. Curr Sci. 2009;96(5):674-82

63. Poole RK. Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation. Anton. Leeuw. 1994;65(4):289-310. https://doi.org/10.1007/BF00872215

64. Fan TWM, Lane AN, Higashi RM. In vivo and in vitro metabolomic analysis of anaerobic rice coleoptiles revealed unexpected pathways. Russ J Plant Physiol. 2003; 50(6):787-93. https://doi.org/10.1023/B:RUPP.0000003276.14947.16

65. Perazzolli M, Romero-Puertas MC, Delledonne M. Modulation of nitric oxide bioactivity by plant hemoglobins. J Exp Bot. 2006; 57(3):479-488. https://doi.org/10.1093/jxb/erj051

66. Igamberdiev AU, Baron K, Manac'h-little N, Stoimenova M, Hill R. The hemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot. 2005; 96(4):557-64. https://doi.org/10.1093/aob/mci210

67. Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. 2004;16(2):332-41. https://doi.org/10.1105/tpc.017822

68. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and mechanisms of nitric oxide. Free Radic Biol Med. 1998;25(4-5):434-56. https://doi.org/10.1016/S0891-5849(98)00092-6

69. Rubio-Cabetas MJ, Pons C, Bielsa B, Amador ML, Marti C, Granell A. Preformed and induced mechanisms underlies the differential responses of Prunus rootstock to hypoxia. J Plant Physiol. 2018;228:134-49. https://doi.org/10.1016/j.jplph.2018.06.004

70. hu X, Li X, Jiu S, Zhang K, Wang C, Fang J. Analysis of the regulation networks in grapevine reveals response to waterlogging stress and candidate gene-marker selection for damage severity. Royal Soc Open Sci. 2018;5:172253. http://dx.doi.org/10.1098/rsos.172253

71. Parthasarathy A, Adams LE, Savka FC, Hudson AO. The Arabidopsis thaliana gene annotated by the locus tag At3g08860 encodes alanine aminotransferase. Plant Direct. 2019; 3(9):e00171. https://doi.org/10.1002/pld3.171

72. Diab H, Limami AM. Reconfiguration of N metabolism upon hypoxia Stress and recovery: roles of alanine aminotransferase (AlaAT) and glutamate dehydrogenase (GDH). Plants. 2016;5(2):25. https://doi.org/10.3390/plants5020025

73. Zeggiani R, Cantu CA, Brambilla I, Bertani A. Accumulation and interconversion of amino acids in rice roots under anoxia. Plant Cell Physiol. 1988;29(6):981-87. https://doi.org/10.1093/oxfordjournals.pcp.a077604

74. Wagner S, Steinbeck J, Fuchs P, Lichtenauer S, Elsasser M, Schippers JHM, Nietzel T, Ruberti C, Aken OV, Dongen JTV, Schmidt RR, Schwarzlander M. Multiparametric real-time sensing of cytosolic physiology linkshypoxia responses to mitochondrial electron transport. New Phytol. 2019; 224(4):1668-84. https://doi.org/10.1111/nph.16093

75. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 2010;15(8):462-70. https://doi.org/10.1016/j.tplants.2010.05.006

76. Lu Y, Wu Y, Han B. Anaerobic Induction of Isocitrate Lyase and Malate Synthase in Submerged Rice Seedlings Indicates the Important Metabolic Role of the Glyoxylate Cycle. Acta Biochim Biophys Sin. 2005;37(6):406-14. https://doi.org/10.1111/j.1745-7270.2005.00060.x

77. Miro B, Ismail AM. Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.). Front Plant Sci. 2013;4:269. https://doi.org/10.3389/fpls.2013.00269

78. Lakshmanan M, Zhang Z, Mohanty B, Kwon J, Choi H, Nam H, Kim D, Lee D. Elucidating rice cell metabolism under flooding and drought stresses using flux-based modeling and analysis. Plant Physiol. 2013;162(4):2140-50. https://doi.org/10.1104/pp.113.220178

79. Yemelyanov VV, Shishova MF, Chirkova TV, Lindberg SM. Anoxia-induced elevation of cytosolic Ca2+ concentration depends on different Ca2+ sources in rice and wheat protoplasts. Planta. 2011;234(2):271-80. https://doi.org/10.1007/s00425-011-1396-x

80. Wang F, Chen Z, Liu X, Colmer TD, Zhou M, Shabala S. Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis. J Exp Bot. 2016;67(12):3747-62. https://doi.org/10.1093/jxb/erw034

81. Schmidt RR, Weits DA, Feulner CFJ, van Dongen JT. 2018. Oxygen sensing and integrative stress signaling in plants. Plant Physiol. 2018;176:1131-42. https://doi.org/10.1104/pp.17.01394

82. He L, Li B, Lu X, Yuan L, Yang Y, Yuan Y, Du J, Guo S. The effect of exogenous calcium on mitochondria, respiratory metabolism enzymes and ion transport in cucumber roots under hypoxia. Sci Rep. 2015;5:11391. https://doi.org/10.1038/srep11391

83. Miyashita Y, Good AG. Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol. 2008;49(1):92-102. https://doi.org/10.1093/pcp/pcm171

84. Subbaiah CC, Zhang J, Sachs MM. Involvement of lntracellular Calcium in Anaerobic Gene Expression and Survival of Maize Seedlings. Plant Physiol. 1994;105(1):369-76. https://doi.org/10.1104/pp.105.1.369

85. Gao H, Jiaa Y, Guoa S, Lv G, Wanga T, Juan L. Exogenous calcium affects nitrogen metabolism in root-zone hypoxia-stressed muskmelon roots and enhances short-term hypoxia tolerance. J Plant Physiol. 2011;168(11):1217-25. https://doi.org/10.1016/j.jplph.2011.01.022

86. Shi K, Ding X, Dong D, Zhou Y, Yu JQ. Putrescine enhancement of tolerance to root-zone hypoxia in Cucumis sativus: a role for increased nitrate reduction. Funct Plant Biol. 2008;35(4):337-45. https://doi.org/10.1071/FP08029

87. Aarnes H, Eriksen AB, Petersen D, Rise F. Accumulation of ammonium in Norway spruce (Picea abies) seedlings measured by in vivo 14N-NMR. J Exp Bot. 2007;58(5):929-34. https://doi.org/10.1093/jxb/erl247

88. Drew MC, He C, Morgan PW. Programmed cell death and aerenchyma formation in roots. Trends Plant Sci. 2000; 5(3):123-27. https://doi.org/10.1016/S1360-1385(00)01570-3

89. Song L, Valliyodan B, Prince S, Wan J, Nguyen HT. Characterization of the XTH Gene Family: New Insight to the Roles in Soybean Flooding Tolerance. Int J Mol Sci. 2018; 19(9):2705. https://doi.org/10.3390/ijms19092705

90. Lemichez E,WuY, Sanchez J, Mettouchi A, Mathur J, Chua N. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev. 2001;15(14):1808-16. https://doi.org/10.1101/gad.900401

91. Sagi M, Fluhr R. Superoxide production by plant homologues of the gp91phox NADPH oxidase. modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 2001;126(3):1281-90. https://doi.org/10.1104/pp.126.3.1281

92. Bailey-Serres J, Baxter-Burrell A, Yang Z, Springer PS. RopGAP4-dependent Rop GTPase Rheostat control of Arabidopsis oxygen deprivation tolerance. Science. 2002; 296(5575):2026-28. https://doi.org/10.1126/science.1071505

93. Steffens B, Sauter M. G proteins as regulators in ethylene-mediated hypoxia signaling. Plant Signaling & Behavior 2010; 5(4):375-78

94. Etherington AM, Hunter MIS, Crawford RMM. Contrasting effects of anoxia on rhizome lipids in Iris species. Phytochem. 1982;21:1275-78. https://doi.org/10.1016/0031-9422(82)80125-8

95. Roberts JKM, Callis J, Jardetzky O, Walbot V, Freeling M. Cytoplasmic acidosis as a determinant of flooding intolerance in plants. PNAS. 1984;81(19):6029-33. https://doi.org/10.1073/pnas.81.19.6029

96. Hanhijarvi AM, Fagerstedt KV. Comparison of the effect of natural and experimental anoxia on carbohydrate and energy metabolism in Iris pseudacorus rhizomes. Physiol Plant. 1994; 90(3):437-44. https://doi.org/10.1111/j.1399-3054.1994.tb08799.x

97. Miller, G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, et al. The plant NADPH Oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2009; 2(84):a45. https://doi.org/10.1126/scisignal.2000448

98. Suzuki N, Koussevitzky S, Mittler R, Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 2012;35(2):259-70. https://doi.org/10.1111/j.1365-3040.2011.02336.x

99. Blokhina OB, Chirkova TV and KV. Fagerstedt. Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot. 2001;52:1179-90. https://doi.org/10.1093/jexbot/52.359.1179

100. Moller IM. Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52: 561-91. https://doi.org/10.1146/annurev.arplant.52.1.561

101. Vergara R, Parada F, Rubio S, Perez FJ. Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J Exp Bot. 2012;63(11):4123-31. https://doi.org/10.1093/jxb/ers094

102. Zhang Y, Ou L, Zhao J, Liu Z, Li X. Transcriptome analysis of hot pepper plants identifies waterlogging resistance related genes. Chil J Agr Res. 2019;79(2):296-306. https://doi.org/10.4067/S0718-58392019000200296

103. Blokhina O, Fagerstedt KV. Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol Bioch. 2010;48(5):359-73. https://doi.org/10.1016/j.plaphy.2010.01.007

104. Noctor G, Foyer CH. Ascorbate and Glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:249-79. https://doi.org/10.1146/annurev.arplant.49.1.249

Published

01-04-2020

How to Cite

1.
Bashar KK, Tareq MZ, Islam MS. Unlocking the mystery of plants’ survival capability under waterlogging stress. Plant Sci. Today [Internet]. 2020 Apr. 1 [cited 2024 May 10];7(2):142-53. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/663

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