渍害胁迫下小麦生长的响应机理及调控措施研究进展

doi:10.13287/j.1001-9332.202012.028

摘要/Abstract

摘要： 全球气候变化导致近年来渍害频发,而旱地作物小麦对渍害敏感。受气候、土壤、轮作制度等因素的影响,我国长江中下游小麦主产区的渍害灾情严重。渍害引起的土壤溶氧量降低可以导致小麦根系生长受到抑制,进而限制植株生长,最终降低小麦产量和品质。本文基于国内外相关研究,从根系呼吸代谢、水分传导、矿质养分吸收、光合作用、氧化还原代谢等方面概述了渍害胁迫抑制小麦生长的生理机理;讨论了小麦通过无氧呼吸维持能量供应和改变根系形态维持氧气供应等渍害适应机制;总结了肥料调控、生长调节剂调控和胁迫记忆等栽培措施在小麦抗渍上的应用及其机理,并对未来小麦抗渍研究进行了展望,以期为小麦的耐渍栽培和稳产高产管理提供理论支撑。

关键词: 小麦, 渍害, 生理机理, 调控措施

Abstract: The frequency of waterlogging events is increasing in recent years due to climate change. Wheat, a dryland crop, is particularly sensitive to waterlogging. Moreover, waterlogging stress is especially serious in the main wheat-producing regions at the middle and lower reaches of the Yangtze River as influenced by regional climate, soil, rotating system and other factors. Oxygen content in soil decreases under waterlogging condition, which inhibits root growth, restricts plant growth, and eventually reduces wheat yield and grain quality. In the present study, we reviewed the current national and international research progress in the underlying physiological mechanisms of inhibitory wheat growth by waterlogging stress, from the aspects of root respiration, water transport, mineral nutrient absorption, photosynthesis, redox metabolism. We discussed the physiological adaptions of wheat to waterlogging, including maintaining energy supply through anaerobic respiration and oxygen supply through changes of root morphology. We listed the application of cultivation measures such as fertilizer regulation, growth regulator regulation and stress memory in improving waterlogging stress-tolerance in wheat with the underlying physiological mechanisms summarized. We also prospected the future study on waterlogging stress-tolerance in wheat, aiming to provide theoretical foundation for waterlogging-tolerant cultivation and maintaining high yield of wheat.

Key words: wheat, waterlogging, physiological mechanism, regulating technique.

高敬文, 苏瑶, 沈阿林. 渍害胁迫下小麦生长的响应机理及调控措施研究进展[J]. 应用生态学报, 2020, 31(12): 4321-4330.

GAO Jing-wen, SU Yao, SHEN A-lin. Research progress of the response mechanism of wheat growth to waterlogging stress and the related regulating managements.[J]. Chinese Journal of Applied Ecology, 2020, 31(12): 4321-4330.

参考文献

[1] 马啸. 2017年全国洪涝灾情综述. 中国防汛抗旱, 2018, 28(8): 60-66 [Ma X. A survey of flood and waterlogging in China in 2017. Flood and Drought Disaster, 2018, 28(8): 60-66]
[2] Nguyen LT, Osanai Y, Anderson IC, et al. Impacts of waterlogging on soil nitrification and ammonia-oxidizing communities in farming system. Plant and Soil, 2018, 426: 299-311
[3] Singh SP, Setter TL. Effect of waterlogging on element concentrations, growth and yield of wheat varieties under farmer's sodic field conditions. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 2017, 87: 513-520
[4] 马尚宇, 王艳艳, 黄正来, 等. 渍水对小麦生长的影响及耐渍栽培技术研究进展. 麦类作物学报, 2019, 39(7): 835-843 [Ma S-Y, Wang Y-Y, Huang Z-L, et al. Research progress of effects of waterlogging on wheat growth and cultivation technique for waterlogging resis-tance. Journal of Triticeae Crops, 2019, 39(7): 835-843]
[5] Herzog M, Striker GG, Colmer TD, et al. Mechanisms of waterlogging tolerance in wheat: A review of root and shoot physiology. Plant, Cell and Environment, 2016, 39: 1068-1086
[6] Manik SN, Pengilley G, Dean G, et al. Soil and crop management practices to minimize the impact of waterlogging on crop productivity. Frontiers in Plant Science, 2019, 10, doi: 10.3389/fpls.2019.00140
[7] Trnka M, Rötter RP, Ruiz-Ramos M, et al. Adverse weather conditions for European wheat production will become more frequent with climate change. Nature Climate Change, 2014, 4: 637-643
[8] 吴洪颜, 张佩, 徐敏, 等. 长江中下游地区冬小麦春季涝渍害灾损风险时空分布特征. 长江流域资源与环境, 2018, 27(5): 1152-1158 [Wu H-Y, Zhang P, Xu M, et al. Spatial-temporal variations of the risk of winter wheat loss suffered from spring waterlogging disaster in the middle and lower Yangtze River reaches. Resources and Environment in the Yangtze Basin, 2018, 27(5): 1152-1158]
[9] 吴洪颜, 曹璐, 李娟, 等. 长江中下游冬小麦春季湿渍害灾损风险评估. 长江流域资源与环境, 2016, 25(8): 1281-1285 [Wu H-Y, Cao L, Li J, et al. Risk assessment on winter wheat suffering from spring wet damages in middle and lower Yangtze. Resources and Environment in the Yangtze Basin, 2016, 25(8): 1281-1285]
[10] 张佩, 吴洪颜, 江海东,等. 长江中下游油菜春季湿渍害灾损风险评估研究. 气象与环境科学, 2019, 42(1): 11-17 [Zhang P, Wu H-Y, Jiang H-D, et al. Risk assessment study on rapeseed suffering from spring wet damages in the middle and lower reaches of Yangtze River. Meteorological and Environmental Sciences, 2019, 42(1): 11-17]
[11] 王利民, 刘佳, 季富华, 等. 中国小麦面积种植结构时空动态变化分析. 中国农学通报, 2019, 35(18): 12-23 [Wang L-M, Liu J, Ji F-H, et al. Analysis of spatial-temporal dynamic change of wheat planting structure of China. Chinese Agricultural Science Bulletin, 2019, 35(18): 12-23]
[12] Ghobadi ME, Ghobadi M, Zebarjadi A. Effect of waterlogging at different growth stages on some morphological traits of wheat varieties. International Journal of Biometeorology, 2017, 61: 635-645
[13] Malik AI, Colmer TD, Lambers H, et al. Short-term waterlogging has long-term effects on the growth and physiology of wheat. New Phytologist, 2002, 153: 225-236
[14] Pang J, Cuin T, Shabala L, et al. Effect of secondary metabolites associated with anaerobic soil conditions on ion fluxes and electrophysiology in barley roots. Plant Physiology, 2007, 145: 266-276
[15] Trought M, Drew M. The development of waterlogging damage in wheat seedlings (Triticum aestivum L.). Plant and Soil, 1980, 54: 77-94
[16] Shao G, Lan J, Yu S, et al. Photosynthesis and growth of winter wheat in response to waterlogging at different growth stages. Photosynthetica, 2013, 51: 429-437
[17] Colmer TD, Greenway H. Ion transport in seminal and adventitious roots of cereals during O₂ deficiency. Journal of Experimental Botany, 2011, 62: 39-57
[18] Yan F, Schubert S, Mengel K. Effect of low root medium pH on net proton release, root respiration, and root growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiology, 1992, 99: 415-421
[19] Cui J, Davanture M, Zivy M, et al. Metabolic responses to potassium availability and waterlogging reshape respiration and carbon use efficiency in oil palm. New Phyto-logist, 2019, 223: 310-322
[20] Mustroph A, Albrecht G. Tolerance of crop plants to oxygen deficiency stress: Fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia. Physiologia Plantarum, 2003, 117: 508-520
[21] Mustroph A, Albrecht G. Fermentation metabolism in roots of wheat seedlings after hypoxic pre-treatment in different anoxic incubation systems. Journal of Plant Physiology, 2007, 164: 394-407
[22] Waters I, Morrell S, Greenway H, et al. Effects of anoxia on wheat seedlings: Ⅱ. Influence of O₂ supply prior to anoxia on tolerance to anoxia, alcoholic fermentation, and sugar levels. Journal of Experimental Botany, 1991, 42: 1437-1447
[23] Phukan UJ, Jeena GS, Tripathi V, et al. MaRAP2-4, a waterlogging-responsive ERF from Mentha, regulates bidirectional sugar transporter At SWEET 10 to modulate stress response in Arabidopsis. Plant Biotechnology Journal, 2018, 16: 221-233
[24] Tan X, Xu H, Khan S, et al. Plant water transport and aquaporins in oxygen-deprived environments. Journal of Plant Physiology, 2018, 227: 20-30
[25] Hamonts K, Clough TJ, Stewart A, et al. Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiology Ecology, 2013, 83: 568-584
[26] Liu F, VanToai T, Moy LP, et al. Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiology, 2005, 137: 1115-1129
[27] Törnroth-Horsefield S, Wang Y, Hedfalk K, et al. Structural mechanism of plant aquaporin gating. Nature, 2006, 439: 688-694
[28] Kamaluddin M, Zwiazek JJ. Metabolic inhibition of root water flow in red-osier dogwood (Cornus stolonifera) seedlings. Journal of Experimental Botany, 2001, 52: 739-745
[29] Zwiazek JJ, Xu H, Tan X, et al. Significance of oxygen transport through aquaporins. Scientific Reports, 2017, 7: 1-11
[30] Qing D, Yang Z, Li M, et al. Quantitative and functional phosphoproteomic analysis reveals that ethylene regulates water transport via the C-terminal phosphorylation of aquaporin PIP2; 1 in Arabidopsis. Molecular Plant, 2016, 9: 158-174
[31] Mahdieh M, Mostajeran A. Abscisic acid regulates root hydraulic conductance via aquaporin expression modulation in Nicotiana tabacum. Journal of Plant Physiology, 2009, 166: 1993-2003
[32] Bramley H, Tyerman S. Root water transport under waterlogged conditions and the roles of aquaporins// Mancuso S, Shabala S, eds. Waterlogging Signalling and Tolerance in Plants. New York: Springer, 2010: 151-180
[33] Elzenga JTM, van Veen H. Waterlogging and plant nutrient uptake// Mancuso S, Shabala S, eds. Waterlogging Signalling and Tolerance in Plants. New York: Springer, 2010: 23-35
[34] Wang F, Chen ZH, Shabala S. Hypoxia sensing in plants: On a quest for ion channels as putative oxygen sensors. Plant and Cell Physiology, 2017, 58: 1126-1142
[35] Kotula L, Clode PL, Striker GG, et al. Oxygen deficiency and salinity affect cell-specific ion concentrations in adventitious roots of barley (Hordeum vulgare). New Phytologist, 2015, 208: 1114-1125
[36] Ylivainio K, Jauhiainen L, Uusitalo R, et al. Waterlogging severely retards P use efficiency of spring barley (Hordeum vulgare). Journal of Agronomy and Crop Science, 2018, 204: 74-85
[37] Marashi SK. Evaluation of uptake rate and distribution of nutrient ions in wheat (Triticum aestivum L.) under waterlogging condition. Plant Physiology, 2018, 8: 2539-2547
[38] Sharma SK, Kulshreshtha N, Kumar A, et al. Waterlogging effects on elemental composition of wheat genotypes in sodic soils. Journal of Plant Nutrition, 2018, 41: 1252-1262
[39] Huang B, Johnson JW, Nesmith S, et al. Growth, phy-siological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply. Journal of Experimental Botany, 1994, 45: 193-202
[40] Wollmer AC, Pitann B, Mühling KH. Timing of waterlogging is crucial for the development of micronutrient deficiencies or toxicities in winter wheat and rapeseed. Journal of Plant Growth Regulation, 2019, 38: 824-830
[41] Wu JD, Li JC, Wei FZ, et al. Effects of nitrogen spraying on the post-anthesis stage of winter wheat under waterlogging stress. Acta Physiologiae Plantarum, 2014, 36: 207-216
[42] Yan K, Zhao S, Cui M, et al. Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. Plant Physio-logy and Biochemistry, 2018, 125: 239-246
[43] Sairam RK, Dharmar K, Lekshmy S, et al. Expression of antioxidant defense genes in mung bean (Vigna radiata L.) roots under water-logging is associated with hypoxia tolerance. Acta Physiologiae Plantarum, 2010, 33: 735-744
[44] 姜东, 陶勤南, 张国平. 渍水对小麦扬麦5号旗叶和根系衰老的影响. 应用生态学报, 2002, 13(11): 1519-1521 [Jiang D, Tao Q-N, Zhang G-P. Effect of waterlogging on senescence of flag leaf and root of wheat Yangmai. Chinese Journal of Applied Ecology, 2002, 13(11): 1519-1521]
[45] Xu QT, Yang L, Zhou ZQ, et al. Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots. Planta, 2013, 238: 969-982
[46] Zaman MSU, Malik AI, Erskine W, et al. Changes in gene expression during germination reveal pea genotypes with either “quiescence” or “escape” mechanisms of waterlogging tolerance. Plant, Cell and Environment, 2019, 42: 245-258
[47] Cannell RQ, Belford RK, Gales K, et al. Effects of waterlogging at different stages of development on the growth and yield of winter wheat. Journal of the Science of Food and Agriculture, 1980, 31: 117-132
[48] Dickin E, Wright D. The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L.). European Journal of Agronomy, 2008, 28: 234-244
[49] Wollmer AC, Pitann B, Mühling KH. Nutrient deficiencies do not contribute to yield loss after waterlogging events in winter wheat (Triticum aestivum). Annals of Applied Biology, 2018, 173: 141-153
[50] Araki H, Hamada A, Hossain MA, et al. Waterlogging at jointing and/or after anthesis in wheat induces early leaf senescence and impairs grain filling. Field Crops Research, 2012, 137: 27-36
[51] Liu Y, Shi CL, Xuan SL, et al. Effects of waterlogging and shading at jointing and grain-filling stages on yield components of winter wheat. International Conference on Computer and Computing Technologies in Agriculture, Beijing, 2015: 1-14
[52] Romina P, Abeledo LG, Miralles DJ. Physiological traits associated with reductions in grain number in wheat and barley under waterlogging. Plant and Soil, 2018, 429: 469-481
[53] Wollmer AC, Pitann B, Mühling KH. Grain storage protein concentration and composition of winter wheat (Triticum aestivum L.) as affected by waterlogging events during stem elongation or ear emergence. Journal of Cereal Science, 2018, 83: 9-15
[54] 冯凯, 王笑, 周琴, 等. 渍水锻炼对下一代小麦花后渍水胁迫下物质积累和转运的影响. 2018中国作物学会学术年会, 扬州, 2018: 83 [Feng K, Wang X, Zhou Q, et al. Effects of waterlogging exercise on matter accumulation and translocation of next generation wheat under waterlogging stress after anthesis. Annual Meeting of the Crop Science Society of China, Yangzhou, 2018: 83
[55] Zhou Q, Wu X, Xin L, et al. Waterlogging and simulated acid rain after anthesis deteriorate starch quality in wheat grain. Plant Growth Regulation, 2018, 85: 257-265
[56] Zhou Q, Huang M, Huang X, et al. Effect of post-anthesis waterlogging on biosynthesis and granule size distribution of starch in wheat grains. Plant Physiology and Biochemistry, 2018, 132: 222-228
[57] Igamberdiev AU, Hill RD. Elevation of cytosolic Ca²⁺ in response to energy deficiency in plants: The general mechanism of adaptation to low oxygen stress. Biochemical Journal, 2018, 475: 1411-1425
[58] Yamauchi T, Colmer TD, Pedersen O, et al. Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. Plant Physiology, 2018, 176: 1118-1130
[59] Guan B. Effect of waterlogging-induced autophagy on programmed cell death in Arabidopsis roots. Frontiers in Plant Science, 2019, 10, doi:10.3389/fpls.2019.00468
[60] Sun L, Ma L, He S, et al. AtrbohD functions downstream of ROP2 and positively regulates waterlogging response in Arabidopsis. Plant Signaling & Behavior, 2018, 13, doi:10.1080/15592324.2018.1513300
[61] Qi X, Li Q, Ma X, et al. Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signaling. Plant, Cell and Environment, 2019, 42: 1458-1470
[62] Yamauchi T, Abe F, Tsutsuimi N, et al. Root cortex provides a venue for gas-space formation and is essential for plant adaptation to waterlogging. Frontiers in Plant Science, 2019, 10, doi:10.3389/fpls.2019.00259
[63] Sundgren TK, Uhlen AK, Lillemo M, et al. Rapid seedling establishment and a narrow root stele promotes waterlogging tolerance in spring wheat. Journal of Plant Physiology, 2018, 227: 45-55
[64] Abiko T, Kotula L, Shiono K, et al. Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant, Cell and Environment, 2012, 35: 1618-1630
[65] Ranathunge K, Lin J, Steudle E, et al. Stagnant deoxygenated growth enhances root suberization and lignifications, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots. Plant, Cell and Environment, 2011, 34: 1223-1240
[66] Armstrong J, Armstrong W. Rice: Sulfide-induced bar-riers to root radial oxygen loss, Fe²⁺ and water uptake, and lateral root emergence. Annals of Botany, 2005, 96: 625-638
[67] Kotula L, Schreiber L, Colmer TD, et al. Anatomical and biochemical characterisation of a barrier to radial O₂ loss in adventitious roots of two contrasting Hordeum marinum accessions. Functional Plant Biology, 2017, 44: 845-857
[68] Kulichikhin K, Yamauchi T, Watanabe K, et al. Biochemical and molecular characterization of rice (Oryza sativa L.)7 roots forming a barrier to radial oxygen loss. Plant, Cell and Environment, 2014, 37: 2406-2420
[69] Noreen S, Fatima Z, Ahmad S, et al. Foliar application of micronutrients in mitigating abiotic stress in crop plants// Hasanuzzaman M, Fujita M, Oku H, eds. Plant Nutrients and Abiotic Stress Tolerance. New York: Springer, 2018: 95-117
[70] Jiang D, Fan XM, Dai TB, et al. Nitrogen fertiliser rate and post-anthesis waterlogging effects on carbohydrate and nitrogen dynamics in wheat. Plant and Soil, 2008, 304: 301-314
[71] Allen DE, Kingston G, Rennenberg H, et al. Effect of nitrogen fertilizer management and waterlogging on nitrous oxide emission from subtropical sugarcane soils. Agriculture, Ecosystems and Environment, 2010, 136: 209-217
[72] Cui J, Abadie C, Carroll A, et al. Responses to K deficiency and waterlogging interact via respiratory and nitrogen metabolism. Plant, Cell and Environment, 2019, 42: 647-658
[73] Najeeb U, Bange MP, Tan DK, et al. Consequences of waterlogging in cotton and opportunities for mitigation of yield losses. AoB Plants, 2015, 7: 1-17
[74] Gill MB, Zeng F, Shabala L, et al. The ability to regulate voltage-gated K⁺-permeable channels in the mature root epidermis is essential for waterlogging tolerance in barley. Journal of Experimental Botany, 2017, 69: 667-680
[75] Wu W, Wang S, Chen H, et al. Optimal nitrogen regimes compensate for the impacts of seedlings subjected to waterlogging stress in summer maize. PLoS One, 2018, 13(10): e0206210
[76] Ren B, Zhang J, Dong S, et al. Exogenous 6-benzyladenine improves antioxidative system and carbon metabolism of summer maize waterlogged in the field. Journal of Agronomy and Crop Science, 2018, 204: 175-184
[77] Kim Y, Seo CW, Khan AL, et al. Exo-ethylene application mitigates waterlogging stress in soybean (Glycine max L.). BMC Plant Biology, 2018, 18: 254
[78] Shiono K, Ejiri M, Shimizu K, et al. Improved waterlogging tolerance of barley (Hordeum vulgare) by pretreatment with ethephon. Plant Production Science, 2019, 22: 285-295
[79] 武辉, 向镜, 陈惠哲, 等. 外源调节剂对淹涝水稻幼苗株高及碳水化合物消耗的影响. 应用生态学报, 2018,29(1): 149-157 [Wu H, Xiang J, Chen H-Z, et al. Effects of exogenous growth regulators on plant elongation and carbohydrate consumption of rice seedlings under submergence. Chinese Journal of Applied Ecology, 2018, 29(1): 149-157]
[80] Yuan LB, Dai YS, Xie LJ, et al. Jasmonate regulates plant responses to postsubmergence reoxygenation through transcriptional activation of antioxidant synthesis. Plant Physiology, 2017, 173: 1864-1880
[81] Zhang Q, Liu X, Zhang Z, et al. Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. Frontiers in Plant Science, 2019, 10, doi: 10.3389/fpls.2019.00044
[82] Andrade CA, de Souza KRD, de Oliveira Santos M, et al. Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. Scientia Horticulturae, 2018, 232: 40-45
[83] Li C, Jiang D, Wollenweber B, et al. Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat. Plant Science, 2011, 180: 672-678
[84] Savchenko T, Rolletschek H, Heinzel N, et al. Waterlogging tolerance rendered by oxylipin-mediated metabolic reprogramming in Arabidopsis. Journal of Experimental Botany, 2019, 70: 2919-2932