Plant Response to Waterlogging Stress: Research Progress

doi:10.11924/j.issn.1000-6850.casb2020-0403

Abstract

Abstract:

Waterlogging stress is an important factor that affects the distribution, growth and development of plants. The research on plant waterlogging tolerance is critical to improving plant tolerance in order to cope with the increasingly severe extreme weather and the large-scale production management. In order to carry out researches on plant waterlogging tolerance and explore the regulation mechanism of different plants in response to waterlogging stress, we summarized the effects of waterlogging stress on plant growth, the regulation mechanism of plant in response to waterlogging stress, and analyzed the effects of waterlogging stress on plant phenotypic traits, biomass, photosynthesis, reactive oxygen species accumulation, sugar content as well as biological membrane in detail. In addition, the regulation mechanism of ethylene signal molecule, reactive oxygen species scavenging mechanism, osmotic regulation, morphological regulation, molecular and metabolic regulation of plant in response to waterlogging stress were also analyzed. Finally, it is proposed that further in-depth study should be focus on the development of exogenous regulatory substances to improve plant waterlogging tolerance.

Key words: waterlogging stress, waterlogging tolerance, response mechanism, phenotype, physiology, molecular

CLC Number:

S332.4

Nie Gongping, Chen Minmin, Yang Liuyan, Cai Youming, Xu Feng, Zhang Yongchun. Plant Response to Waterlogging Stress: Research Progress[J]. Chinese Agricultural Science Bulletin, 2021, 37(18): 57-64.

References 80

[1]	Herzog M, Striker G G, Colmer T D, et al. Mechanisms of waterlogging tolerance in wheat -a review of root and shoot physiology[J]. Plant Cell & Environment, 2016,39(5):1068-1086.
[2]	Arguello M N, Mason R E, Roberts T L, et al. Performance of soft red winter wheat subjected to field soil waterlogging: Grain yield and yield components[J]. Field Crops Research, 2016: 57-64.
[3]	Zhang Y, Chen Y, Lu H, et al. Growth, lint yield and changes in physiological attributes of cotton under temporal waterlogging[J]. Field Crops Research, 2016: 83-93.
[4]	尹冬梅, 管志勇, 陈素梅, 等. 菊花及其近缘种属植物耐涝评价体系建立及耐涝性鉴定[J]. 植物遗传资源学报, 2009,10(3):399-404.
[5]	宋钊, 张白鸽, 李颖, 等. 辣椒形态学耐涝评价体系的建立与应用[J]. 热带作物学报, 2017,038(10):1815-1822.
[6]	Loreti E, van Veen H, Perata P. Plant responses to flooding stress[J]. Current Opinion in Plant Biology. 2016,33:64-71. doi: S1369-5266(16)30088-7 pmid: 27322538
[7]	Minami A, Yano K, Gamuyao R, et al. Time-Course Transcriptomics Analysis Reveals Key Responses of Submerged Deepwater Rice to Flooding[J]. Plant Physiology. 2018,176(4):3081-3102. doi: 10.1104/pp.17.00858 pmid: 29475897
[8]	Peng Y, Zhou Z, Zhang Z, et al. Molecular and physiological responses in roots of two full-sib poplars uncover mechanisms that contribute to differences in partial submergence tolerance[J]. Scientific Reports, 2018,8(1):12829. doi: 10.1038/s41598-018-30821-y URL
[9]	Arbona V, Hossain Z, María F López-Climent, et al. Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[J]. Physiologia Plantarum, 2008,132(4):452-466. doi: 10.1111/j.1399-3054.2007.01029.x URL
[10]	Yetisir H, Aliskan M E, Soylu S, et al. Some physiological and growth responses of watermelon [Citrullus lanatus (Thunb.) Matsum. and Nakai] grafted onto Lagenaria siceraria to flooding[J]. Environmental & Experimental Botany, 2006,58(1-3):1-8.
[11]	Zeng N, Yang Z, Zhang Z, et al. Comparative transcriptome combined with proteome analyses revealed key factors involved in alfalfa (Medicago sativa) response to waterlogging stress[J]. International Journal of Molecular Sciences, 2019,20(6):1359. doi: 10.3390/ijms20061359 URL
[12]	Wei W, Li D, Wang L, et al. Morpho-anatomical and physiological responses to waterlogging of sesame (Sesamum indicum L.)[J]. Plant Science, 2013,208(Complete):102-111. doi: 10.1016/j.plantsci.2013.03.014 URL
[13]	Anee T I, Nahar K, Rahman A, et al. Oxidative Damage and Antioxidant Defense in Sesamum indicum after Different Waterlogging Durations[J]. Plants (Basel), 2019,8(7):196.
[14]	Castonguay Y, Nadeau P, Simard R R. Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa[J]. Plant Cell and Environment, 1993,16:695-702. doi: 10.1111/pce.1993.16.issue-6 URL
[15]	Barickman T C, Simpson C R, Sams C E. Waterlogging Causes Early Modification in the Physiological Performance, Carotenoids, Chlorophylls, Proline, and Soluble Sugars of Cucumber Plants[J]. Plants (Basel), 2019,8(6) pii:E160
[16]	Huang B, Nesmith D S, Bridges D C, et al. Responses of squash to salinity, waterlogging, and subsequent drainage: II. Root and shoot growth[J]. Journal of Plant Nutrition 1995,18(1):141-152. doi: 10.1080/01904169509364891 URL
[17]	Malik A I, Colmer T D, Lambers H, et al. Short-term waterlogging has long-term effects on the growth and physiology of wheat[J]. New Phytololgy, 2002,153:225-236.
[18]	Ezin Vincent, Pena Robert De La, Ahanchede Adam, et al. Flooding tolerance of tomato genotypes during vegetative and reproductive stages[J]. Plant Physiololgy, 2010,22:131-142.
[19]	Perl-Treves R, Perl A. Oxidative stress: an introduction.In: Inze´ D, Montagu MV (eds) Oxidative Stress in Plants[M]. London: Taylor & Francis, 2002: 1-32.
[20]	Blokhina O, Virolainen E, Fagerstedt K V, et al. Antioxidants, oxidative damage and oxygen deprivation stress: a review[J]. Annals of Botany, 2003,91:179-194. doi: 10.1093/aob/mcf118 URL
[21]	Alam I, Lee D G, Kim K H, et al. Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage[J]. Journal of Bioences, 2010,35(1):49-62.
[22]	Sairam R K, Kumutha D, Chinnusamy V, et al. Waterlogging- induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata)[J]. Journal of Plant Physiololgy, 2009,166:602-616.
[23]	Zeng Y, Avigne W T, Koch K E, et al. Rapid repression of maize invertase by low oxygen: Invertase/sucrose synthase balance, sugar signaling potential and seedling survival[J]. Plant Physiololgy, 1999,121:599-608.
[24]	Albrecht G, Mustroph A, Fox T C, et al. Sugar and fructan accumulation during metabolic adjustment between respiration and fermentation under low oxygen conditions in wheat roots[J]. Plant Physiololgy, 2004,120:93-105.
[25]	Mustroph A, Albrecht G. Tolerance of crop plants to oxygen deficiency stress: fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia[J]. Physiologia Plantarum, 2003,117:508-520. doi: 10.1034/j.1399-3054.2003.00051.x URL
[26]	Huang B, Johnson J W. Root respiration and carbohydrate status of two wheat genotypes in response to hypoxia[J]. Annals of Botany, 1995,75:427-432. doi: 10.1006/anbo.1995.1041 URL
[27]	杨曼, 张佑麟, 徐振东, 等. 水分胁迫对黑壳楠和香樟幼苗生理特性的影响[J]. 南方农业学报, 2015,46(8):1449-1454.
[28]	庞宏东, 胡兴宜, 胡文杰, 等. 淹水胁迫对枫杨等3个树种生理生化特性的影响[J]. 中国林业科技大学学报, 2018,38(10):15-20.
[29]	Voesenek L, Bailey-Serres J. Flooding tolerance: O₂ sensing and survival strategies[J]. Current Opinion in Plant Biology, 2013,16:647-653. doi: 10.1016/j.pbi.2013.06.008 pmid: 23830867
[30]	Jackson M B, Colmer T D. Response and adaptation by plants to flooding stress[J]. Annals of Botany, 2005,96:501-505. doi: 10.1093/aob/mci205 URL
[31]	Justin S H F W, Armstrong W. The anatomical characteristics of roots and plant response to soil flooding[J]. New Phytololgy, 1987,106:465-495.
[32]	Evans D E. Aerenchyma formation[J]. New Phytololgy, 2003,161:35-49.
[33]	Jackson M B. Ethylene and responses of plants to soil waterlogging and submergence[J]. Annual Review Plant Physiololgy, 1985,36:145-174.
[34]	Stünzi J T, Kende H. Gas composition in the internal air spaces of deep water rice in relation to growth induced by submergence[J]. Plant and Cell Physiololgy, 1989,30:49-56.
[35]	Sairam R K, Kumutha D, Ezhilmathi K, et al. physiology and biochemistry of waterlogging tolerance in plants[J]. Biologia Plantarum, 2008,52(3):401-412. doi: 10.1007/s10535-008-0084-6 URL
[36]	Visser E J W, Bogemann G, Blom C W P M, et al. Ethylene accumulation in waterlogged Rumex plants promotes formation of adventitious roots[J]. Journal of experimental Botany, 1996,47:403-410. doi: 10.1093/jxb/47.3.403 URL
[37]	Davies D D. Anaerobic metabolism and the production of organic acids. In: Davies DD (ed) The biochemistry of plants[M]. New York: Academic Press, 1980: 581-611.
[38]	Jackson M B, Drew M C. Effects of flooding on growth and metabolism of herbaceous plants. In: Kozlowski TT (ed) Flooding and plant growth[M]. New York: Academic Press, 1984: 47-128.
[39]	Ashraf M. Biotechnological approach of improving plant salt tolerance using antioxidants as markers[J]. Biotechnology Advances, 2009,27:84-93. doi: 10.1016/j.biotechadv.2008.09.003 pmid: 18950697
[40]	Mittler R, Vanderauwera S, Gollery M, et al. Reactive oxygen gene network of plants[J]. Trends in Plant Science, 2004,9:490-498. doi: 10.1016/j.tplants.2004.08.009 URL
[41]	Narayanan S, Ruma D, Gitika B, et al. Antioxidant activities of seabuckthorn (Hippophae rhamnoides) during hypoxia induced oxidative stress in glial cells[J]. Molecular and Cellular Biochemistry, 2005,278:9-14. doi: 10.1007/s11010-005-7636-2 URL
[42]	Foyer C H, Looez-Delgado H, Dat J F, et al. Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling[J]. Physiologia Plantarum, 1997,100:241-254. doi: 10.1111/ppl.1997.100.issue-2 URL
[43]	Garnczarska M. Response of the ascorbate-glutathione cycle to re-aeration following hypoxia in lupine roots[J]. Plant Physiology and Biochemistry, 2005,43:583-590. pmid: 15975806
[44]	Bradford K J N D, Yang S F. Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants[J]. Plant Physiololgy, 1980,65:322-326.
[45]	Cohen E, Kende H. In vivo 1-aminocyclopropane-1-carboxylate synthase activity in internodes of deep water rice: Enhancement by submergence and low oxygen levels[J]. Plant Physiololgy, 1987,84:282-286.
[46]	Geisler-Lee J, Caldwell C, Gallie D R, et al. Expression of the ethylene biosynthetic machinery in maize roots is regulated in response to hypoxia[J]. Journal of Experimental Botany, 2010,61:857-871. doi: 10.1093/jxb/erp362 pmid: 20008461
[47]	Vriezen W H, Hulzink R, Mariani C, et al. 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynjournal in Rumex palustris during submergence[J]. Plant Physiololgy, 1999,121:189-196.
[48]	Emuejevoke V, Onyekachukwu A, El-Esawi M A, , et al. Comparative physiological, biochemical, and genetic responses to prolonged waterlogging stress in okra and maize given exogenous ethylene priming[J]. Frontiers in Physiology, 2017,8:632. doi: 10.3389/fphys.2017.00632 pmid: 28993735
[49]	Lin K H R, Tsou C C, Hwang S Y, et al. Paclobutrazol pre-treatment enhanced flooding tolerance of sweet potato[J]. Journal of Plant Physiololgy, 2006,163:750-760.
[50]	Ushimaro T, Shibasaka M, Tsuji H. Development of O₂- detoxification system during adaptation to air of submerged rice seedlings[J]. Plant and Cell Physiology, 1992,33:1065-1071.
[51]	Hurng W P, Kao C H. Effect of flooding on the activities of some enzymes of activated oxygen metabolism, the levels of antioxidants, and lipid peroxidation in senescencing tobacco leaves[J]. Plant Growth Regulation, 1994,14:37-44. doi: 10.1007/BF00024139 URL
[52]	Hurng W P, Kao C H. Lipid peroxidation and antioxidative enzymes in senesencing tobacco leaves following flooding[J]. Plant Science, 1994,96:41-44. doi: 10.1016/0168-9452(94)90220-8 URL
[53]	Hwang S Y, Lo H F, hao C K, et al. Changes in antioxidative enzyme activities in two leafy vegetable sweet potato cultivars subjected to waterlogged conditions[J]. Journal of the China Society for Horticultural Science, 2000,46:287-296.
[54]	Ahmed S, Nawata E, Hosokawa M, et al. Alterations in photosynjournal and some antioxidant enzymatic activities of mungbean subjected to waterlogging[J]. Plant Science, 2000,163:117-123. doi: 10.1016/S0168-9452(02)00080-8 URL
[55]	Grassini P, Indaco G V, Pereira M L, et al. Responses to shortterm waterlogging during grain filling in sunflower[J]. Field Crops Research, 2007,101:352-363 doi: 10.1016/j.fcr.2006.12.009 URL
[56]	Li C, Jiang D, Wollenweber B, et al. Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anjournal in wheat[J]. Plant Science, 2011,180:672-678. doi: 10.1016/j.plantsci.2011.01.009 URL
[57]	Yordanova R Y, Christov K N, Popova L P. Antioxidative enzymes in barley plants subjected to soil flooding[J]. Environmental and Experimental Botany, 2004,51:93-101. doi: 10.1016/S0098-8472(03)00063-7 URL
[58]	Yordanova R Y, Popova L P. Photosynthetic Response of Barley Plants to Soil Flooding[J]. Photosynthetica (Prague), 2001,39(4):515-520.
[59]	梁芳, 黄寿镕, 於艳萍, 等. 红花玉蕊对淡水全淹胁迫的生长及生理响应[J]. 西南林业大学学报, 201939(3):18-25.
[60]	Drew M C, He C J, Morgan P W. Programmed cell death and aerenchyma formation in roots[J]. Trends in Plant Science, 2000,5(3):123-127. doi: 10.1016/S1360-1385(00)01570-3 URL
[61]	Jiang Z, Song X F, Zhou Z Q, et al. Aerenchyma formation: programmed cell death in adventitious roots of winter wheat (Triticum aestivum) under waterlogging[J]. Functional Plant Biology, 2010,37(8):748-755. doi: 10.1071/FP09252 URL
[62]	Zhao N, Li C, Yan Y, et al. Comparative Transcriptome Analysis of Waterlogging-Sensitive and Chrysanthemum morifolium Cultivars under Waterlogging Stress and Reoxygenation Waterlogging-Tolerant Chrysanthemum morifolium Cultivars under Waterlogging Stress and Reoxygenation Conditions[J]. Internaltional Journal of Molecular Science, 2018,19.
[63]	Ayano M, Kani T, Kojima M, et al. Gibberellin biosynjournal and signal transduction is essential for internode elongation in deepwater rice[J]. Plant Cell and Environment, 2015,37:2313-2324. doi: 10.1111/pce.2014.37.issue-10 URL
[64]	Schmitz A J, Folsom J J, Jikamaru Y, et al. SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway[J]. New Phytologist, 2013,198:1060-1070. doi: 10.1111/nph.2013.198.issue-4 URL
[65]	Kim Y H, Hwang S J, Waqas M, et al. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance[J]. Frontiers in Plant Science, 2015,6:714.
[66]	Zeng B, Zhang Y, Zhang A, et al. Transcriptome profiling of two Dactylis glomerata L. cultivars with different tolerance in response to submergence stress[J]. Phytochemistry, 2020,175:112378. doi: 10.1016/j.phytochem.2020.112378 URL
[67]	Chugh V, Gupta A K, Grewal M S, et al. Response of antioxidative and ethanolic fermentation enzymes in maize seedlings of tolerant and sensitive genotypes under short-term waterlogging[J]. Indian Journal Experimental Biology, 2012,50:577-582.
[68]	Fukao T, Bailey-Serres J. Plant responses to hypoxia - is survival a balancing act[J]. Trends in Plant Science, 2004,9:449-456. doi: 10.1016/j.tplants.2004.07.005 URL
[69]	Kumutha D, Sairam R K, Ezhilmathi K, et al. Effect of waterlogging on carbohydrate metabolism in pigeon pea (Cajanus cajan L.): upregulation of sucrose synthase and alcohol dehydrogenase[J]. Plant Science, 2008,175:706-716. doi: 10.1016/j.plantsci.2008.07.013 URL
[70]	Ismail A M, Ella E S, Vergara G V, et al. Mechanisms associated with tolerance of flooding during germination and early seedling growth in rice (Oryza sativa)[J]. Annals of Botany, 2009,103:197-209. doi: 10.1093/aob/mcn211 URL
[71]	Ismond K P, Dolferus R, Pauw M, et al. Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway[J]. Plant Physiology, 2003,132:1292-1302. doi: 10.1104/pp.103.022244 URL
[72]	Ren B, Dong S, Zhao B, et al. Responses of Nitrogen Metabolism, Uptake and Translocation of Maize to Waterlogging at Different Growth Stages[J]. Frontiers in Plant Science, 2017,8:1216. doi: 10.3389/fpls.2017.01216 URL
[73]	Borrego-Benjumea A, Carter A, Tucker J R, et al. Genome-Wide Analysis of Gene Expression Provides New Insights into Waterlogging Responses in Barley (Hordeum vulgare L.)[J]. Plants (Basel), 2020,9(2):240.
[74]	Fu S, Chang P L, Friesen M L, et al. Identifying similar transcripts in a related organism from de Bruijn graphs of RNA-Seq data, with applications to the study of salt and waterlogging tolerance in Melilotus[J]. BMC Genomics, 2019,20(Suppl 5):425. doi: 10.1186/s12864-019-5702-5 URL
[75]	López-Delgado H A, Martínez-Gutiérrez R, Mora-Herrera M E, et al. Induction of freezing tolerance by the application of hydrogen peroxide and salicylic acid as tuber-dip or canopy spraying in Solanum tuberosum L.[J]. Potato Research, 2018,61:195-206. doi: 10.1007/s11540-018-9368-1 URL
[76]	İşeri Ö D, Körpe D A, Sahin F I, et al. Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress[J]. Acta Physiologiae Plantarum, 2013,35:1905-1913. doi: 10.1007/s11738-013-1228-7 URL
[77]	Khan T A, Yusuf M, Fariduddin Q. Seed treatment with H₂O₂ modifies net photosynthetic rate and antioxidant system in mung bean (Vigna radiata L. Wilczek) plants[J]. Israel Journal of Plant Science, 2015,62:167-175. doi: 10.1080/07929978.2015.1060806 URL
[78]	Bhattacharjee S. An inductive pulse of hydrogen peroxide pretreatment restores redox-homeostasis and oxidative membrane damage under extremes of temperature in two rice cultivars[J]. Plant Growth Regulation, 2012,68:395-410. doi: 10.1007/s10725-012-9728-9 URL
[79]	Guzel S, Terzi R. Exogenous hydrogen peroxide increases dry matter production, mineral content and level of osmotic solutes in young maize leaves and alleviates deleterious effects of copper stress[J]. Botanical Studies, 2013,54(1):26. doi: 10.1186/1999-3110-54-26 URL
[80]	Andrade C A, de Souza K R D, Santos M D O, et al. Hydrogen peroxide promotes the tolerance of soybeans to waterlogging[J]. Scientia Horticulturae, 2018,232:40-45. doi: 10.1016/j.scienta.2017.12.048 URL