Abstract
The impact of waterlogging on crops has increased during the last decades due to climate change, being considered the second most important abiotic stress after drought in soybean, with yield reductions of up to 80%. In this review, we performed a quantitative review from 54 papers about waterlogging effects in soybean. Yield losses are greater (57%) with waterlogging occurring at reproductive stages between R1 and R3 compared to vegetative stages, which is mostly related to a diminished number of pods per plant. Waterlogging impacts on biological nitrogen fixation, with losses of about 30 and 50% in nodule number and weight, with the greatest reductions in reproductive stages. The nitrogenase activity is drastically reduced with water excess but can quickly restore after. Losses in photosynthesis are about 30–50%, mostly related to reduced stomatal conductance and poor N status. Soybean can also develop aerenchymatous tissue in roots, hypocotyls and nodules, which may alleviate the anoxia generated by waterlogging by facilitating oxygen transport. Further efforts should be invested in investigating the effect of waterlogging on nodulation and the impact and subsequent recovery of root growth.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
Not applicable.
Code availability
Not applicable.
References
Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) 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 Environ 35:1618–1630. https://doi.org/10.1111/j.1365-3040.2012.02513.x
Aggarwal PK, Kalra N, Chander S, Pathak H (2006) InfoCrop: a dynamic simulation model for the assessment of crop yields, losses due to pests, and environmental impact of agro-ecosystems in tropical environments. I. Model description. Agric Syst 89:1–25. https://doi.org/10.1016/j.agsy.2005.08.001
Andrade CA, de Souza KRD, de Oliveira Santos M, da Silva DM, Alves JD (2018) Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. Sci Hortic 232:40–45. https://doi.org/10.1016/j.scienta.2017.12.048
Ara R, Mannan MA, Khaliq QA, Miah MU (2015) Waterlogging tolerance of soybean. Bangladesh Agron J 18:105–109
Araki H (2006) Water uptake of soybean (Glycine max L. Merr.) during exposure to O2 deficiency and field level CO2 concentration in the root zone. Field Crops Res 96:98–105. https://doi.org/10.1016/j.fcr.2005.05.007
Asseng S, Cao W, Zhang W, Ludwig F (2009) Crop physiology, modelling and climate change: Impact and adaptation strategies. In: Sadras VO, Calderini DF (eds) Crop physiology: applications for genetic improvement and agronomy. Elsevier Academic Press, Cambridge, pp 511–543
Bacanamwo M, Purcell LC (1999a) Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. J Exp Bot 50:689–696. https://doi.org/10.1093/jxb/50.334.689
Bacanamwo M, Purcell LC (1999b) Soybean root morphological and anatomical traits associated with acclimation to flooding. Crop Sci 39:143–149. https://doi.org/10.2135/cropsci1999.0011183X003900010023x
Boote KJ, Gallaher RN, Robertson WK, Hinson K, Hammond LC (1978) Effect of Foliar Fertilization on Photosynthesis, Leaf Nutrition, and Yield of Soybeans 1. Agron J 70:787–791. https://doi.org/10.2134/agronj1978.00021962007000050022x
Buttery BR (1987) Some effects of waterlogging and supply of combined nitrogen on soybean growth. Can J Plant Sci 67:69–77. https://doi.org/10.4141/cjps87-008
Calvin, Damanik RI, Siregar LAM (2019) Growth and production of soybean (Glycine max L. Merril) varieties in response to waterlogging at vegetative (V5) growth phase by application of gibberellic acid and salicylic acid. In: IOP Conference Series: Earth and Environmental Science (Vol. 260, No. 1, p. 012143). IOP Publishing
Cho JW, Yamakawa T (2006) Comparison of photosynthetic response of two soybean cultivars to soil flooding. J Fac Agr Kyushu Univ 51:227–232
Collaku A, Harrison SA (2002) Losses in wheat due to waterlogging. Crop Sci 42:444–450. https://doi.org/10.2135/cropsci2002.4440
Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36. https://doi.org/10.1046/j.1365-3040.2003.00846.x
da-Silva CJ, do Amarante L (2020) Short-term nitrate supply decreases fermentation and oxidative stress caused by waterlogging in soybean plants. Environ Exp Bot 176:104078. https://doi.org/10.1016/j.envexpbot.2020.104078
de Marcos Lapaz A, de Camargos LS, Yoshida CHP, Firmino AC, de Figueiredo PAM, Aguilar JV, Tomaz RS (2020) Response of soybean to soil waterlogging associated with iron excess in the reproductive stage. Physiol Mol Biol Plants 26:1635–1648. https://doi.org/10.1007/s12298-020-00845-8
Divito GA, Echeverría HE, Andrade FH, Sadras VO (2015) Diagnosis of S deficiency in soybean crops: Performance of S and N: S determinations in leaf, shoot and seed. Field Crops Res 180:167–175. https://doi.org/10.1016/j.fcr.2015.06.006
FAO (2019) Food and Agriculture Organization of the United Nations [FAO]. Retrieved from: https://www.fao.org/faostat/en/#data/QCL
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Fehr WR, Caviness CE (1977) Stages of soybean development. Iowa State University. https://lib.dr.iastate.edu/specialreports/87
Garcia N, da-Silva CJ, Cocco KLT, Pomagualli D, de Oliveira FK, da Silva JVL, do Amarante L (2020) Waterlogging tolerance of five soybean genotypes through different physiological and biochemical mechanisms. Environ Exp Botany 172:103975. https://doi.org/10.1016/j.envexpbot.2020.103975
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212. https://doi.org/10.1016/j.plaphy.2013.05.032
Githiri SM, Watanabe S, Harada K, Takahashi R (2006) QTL analysis of flooding tolerance in soybean at an early vegetative growth stage. Plant Breed 125:613–618. https://doi.org/10.1111/j.1439-0523.2006.01291.x
Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007a) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: I. Root and nodule development. J Agron Crop Sci 193:177–188. https://doi.org/10.1111/j.1439-037X.2007.00257.x
Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007b) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: II. Aboveground growth and biomass. J Agron Crop Sci 193:189–197. https://doi.org/10.1111/j.1439-037X.2007.00258.x
Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kanae S (2013) Global flood risk under climate change. Nat Clim Chang 3:816–821. https://doi.org/10.1038/nclimate1911
Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420. https://doi.org/10.3389/fpls.2015.00420
Inzé D, Van Montagu M (1995) Oxidative stress in plants. Curr Opin Biotechnol 6:153–158. https://doi.org/10.1016/0958-1669(95)80024-7
Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287. https://doi.org/10.1055/s-2007-978516
James EK, Crawford RMM (1998) Effect of oxygen availability on nitrogen fixation by two Lotus species under flooded conditions. J Exp Bot 49:599–609. https://doi.org/10.1093/jxb/49.320.599
Jitsuyama Y (2017) Hypoxia-responsive root hydraulic conductivity influences soybean cultivar-specific waterlogging tolerance. Am J Plant Sci 8:770. https://doi.org/10.4236/ajps.2017.84054
Jung G, Matsunami T, Oki Y, Kokubun M (2008) Effects of waterlogging on nitrogen fixation and photosynthesis in supernodulating soybean cultivar Kanto 100. Plant Prod Sci 11:291–297. https://doi.org/10.1626/pps.11.291
Kaur G, Singh G, Motavalli PP, Nelson KA, Orlowski JM, Golden BR (2020) Impacts and management strategies for crop production in Waterlogged/Flooded soils: A review. Agron J 112:1475–1501. https://doi.org/10.1002/agj2.20093
Keister DL, Rao VR (1977) Nitrogen fixation in Rhizobium japonicum x planta. In: Recent developments in nitrogen fixation. Academic, New York, pp 419–430
Kim YH, Hwang SJ, Waqas M, Khan AL, Lee JH, Lee JD, Lee IJ (2015) Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front Plant Sci 6:714. https://doi.org/10.3389/fpls.2015.00714
Kim Y, Seo CW, Khan AL, Mun BG, Shahzad R, Ko JW, Lee IJ (2018) Exo-ethylene application mitigates waterlogging stress in soybean (Glycine max L.). BMC Plant Biol 18:1–16. https://doi.org/10.1186/s12870-018-1457-4
Kim KH, Cho MJ, Kim JM, Lee T, Heo JH, Jeong JY, Kang S (2019) Growth response and developing simple test method for waterlogging stress tolerance in soybean. J Crop Sci Biotechnol 22:371–378. https://doi.org/10.1007/s12892-019-0271-0
Konnerup D, Toro G, Pedersen O, Colmer TD (2018) Waterlogging tolerance, tissue nitrogen and oxygen transport in the forage legume Melilotus siculus: a comparison of nodulated and nitrate-fed plants. Ann Bot 121:699–709. https://doi.org/10.1093/aob/mcx202
Lamptey S, Ahiabor BDK, Yeboah S, Osei D (2014) Effect of Rhizobium Inoculants and Reproductive Growth Stages on Shoot Biomass and Yield of Soybean. J Agric Sci 6:44–54 http://hdl.handle.net/123456789/1067
Linkemer G, Board JE, Musgrave ME (1998) Waterlogging effects on growth and yield components in late-planted soybean. Crop Sci 38:1576–1584. https://doi.org/10.2135/cropsci1998.0011183X003800060028x
Loureiro MF, James EK, Sprent JI, Franco AA (1995) Stem and root nodules on the tropical wetland legume Aeschynomene fluminensis. New Phytol 130:531–544. https://doi.org/10.1111/j.1469-8137.1995.tb04330.x
Maekawa T, Shimamura S, Shimada S (2011) Effects of short-term waterlogging on soybean nodule nitrogen fixation at different soil reductions and temperatures. Plant Prod Sci 14:349–358. https://doi.org/10.1626/pps.14.349
Mammadov J, Buyyarapu R, Guttikonda SK, Parliament K, Abdurakhmonov IY, Kumpatla SP (2018) Wild relatives of maize, rice, cotton, and soybean: treasure troves for tolerance to biotic and abiotic stresses. Front Plant Sci 9:886. https://doi.org/10.3389/fpls.2018.00886
Mano Y, Omori F (2013) Flooding tolerance in interspecific introgression lines containing chromosome segments from teosinte (Zea nicaraguensis) in maize (Zea mays subsp. mays). Ann Bot 112:1125–1139. https://doi.org/10.1093/aob/mct160
Matsunami T, Jung GH, Oki Y, Kokubun M (2007) Effect of waterlogging during vegetative stage on growth and yield in supernodulating soybean cultivar sakukei 4. Plant Prod Sci 10:112–121. https://doi.org/10.1626/pps.10.112
Minchin FR, Pate JS (1975) Effects of water, aeration, and salt regime on nitrogen fixation in a nodulated legume—definition of an optimum root environment. J Exp Bot 26:60–69. https://doi.org/10.1093/jxb/26.1.60
Momen NN, Carlson RE, Shaw RH, Arjmand O (1979) Moisture-Stress Effects on the Yield Components of Two Soybean Cultivars 1. Agron J 71:86–90. https://doi.org/10.2134/agronj1979.00021962007100010022x
Nguyen VL, Vuong TD, VanToai T, Lee JD, Wu X, Mian MR, Nguyen HT (2012) Mapping of quantitative trait loci associated with resistance to Phytophthora sojae and flooding tolerance in soybean. Crop Sci 52:2481–2493. https://doi.org/10.2135/cropsci2011.09.0466
Nguyen VL, Takahashi R, Githiri SM, Rodriguez TO, Tsutsumi N, Kajihara S, Mochizuki T (2017) Mapping quantitative trait loci for root development under hypoxia conditions in soybean (Glycine max L. Merr.). Theor Appl Genet 130:743–755. https://doi.org/10.1007/s00122-016-2847-3
Nguyen VL, Dang TTH, Chu HD, Nakamura T, Abiko T, Mochizuki T (2021) Near-isogenic lines of soybean confirm a QTL for seed waterlogging tolerance at different temperatures. Euphytica 217:1–10. https://doi.org/10.1007/s10681-020-02736-1
Olivares J, Bedmar EJ, Sanjuán J (2013) Biological nitrogen fixation in the context of global change. Mol Plant-Microbe Interact 26:486–494. https://doi.org/10.1094/MPMI-12-12-0293-CR
Oosterhuis DM, Scott HD, Hampton RE, Wullschleger SD (1990) Physiological responses of two soybean [Glycine max (L.) Merr] cultivars to short-term flooding. Environ Exp Bot 30:85–92. https://doi.org/10.1016/0098-8472(90)90012-S
Pantin F, Monnet F, Jannaud D, Costa JM, Renaud J, Muller B, Genty B (2013) The dual effect of abscisic acid on stomata. New Phytol 197:65–72. https://doi.org/10.1111/nph.12013
Parvin S, Uddin S, Tausz-Posch S, Armstrong R, Tausz M (2020) Carbon sink strength of nodules but not other organs modulates photosynthesis of faba bean (Vicia faba) grown under elevated [CO2] and different water supply. New Phytol 227:132–145. https://doi.org/10.1111/nph.16520
Pedersen O, Nakayama Y, Yasue H, Kurokawa Y, Takahashi H, Heidi Floytrup A, Nakazono M (2021) Lateral roots, in addition to adventitious roots, form a barrier to radial oxygen loss in Zea nicaraguensis and a chromosome segment introgression line in maize. New Phytol 229:94–105. https://doi.org/10.1111/nph.16452
Pedó T, Koch F, Martinazzo EG, Villela FA, Aumonde TZ (2015) Physiological attributes, growth and expression of vigor in soybean seeds under soil waterlogging. Afr J Agric Res 10:3791–3797. https://doi.org/10.5897/AJAR2015.9661
Pereira YC, Silva FRD, Silva BRSD, Cruz FJR, Marques DJ, Lobato AKDS (2020) 24-epibrassinolide induces protection against waterlogging and alleviates impacts on the root structures, photosynthetic machinery and biomass in soybean. Plant Signal Behav 15:1805885. https://doi.org/10.1080/15592324.2020.1805885
Phukan UJ, Mishra S, Shukla RK (2016) Waterlogging and submergence stress: affects and acclimation. Crit Rev Biotechnol 36:956–966. https://doi.org/10.3109/07388551.2015.1064856
Poorter H, Fiorani F, Pieruschka R, Wojciechowski T, van der Putten WH, Kleyer M, Postma J (2016) Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field. New Phytol 212:838–855. https://doi.org/10.1111/nph.14243
Rhine MD, Stevens G, Shannon G, Wrather A, Sleper D (2010) Yield and nutritional responses to waterlogging of soybean cultivars. Irrig Sci 28:135–142. https://doi.org/10.1007/s00271-009-0168-x
Roberts DM, Choi WG, Hwang JH (2010) Strategies for adaptation to waterlogging and hypoxia in nitrogen fixing nodules of legumes. In: Waterlogging signalling and tolerance in plants. Springer, pp. 37–59. https://doi.org/10.1007/978-3-642-10305-6_3
Sallam A, Scott HD (1987) Effects of prolonged flooding on soybeans during early vegetative growth1. Soil Sci 144:61–66
Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: A meta-analysis. Field Crops Res 240:106–115. https://doi.org/10.1016/j.fcr.2019.05.006
Scott HD, DeAngulo J, Daniels MB, Wood LS (1989) Flood duration effects on soybean growth and yield. Agron J 81:631–636. https://doi.org/10.2134/agronj1989.00021962008100040016x
Shi F, Yamamoto R, Shimamura S, Hiraga S, Nakayama N, Nakamura T, Komatsu S (2008) Cytosolic ascorbate peroxidase 2 (cAPX 2) is involved in the soybean response to flooding. Phytochemistry 69:1295–1303. https://doi.org/10.1016/j.phytochem.2008.01.007
Shimamura S, Mochizuki T, Nada Y, Fukuyama M (2002) Secondary aerenchyma formation and its relation to nitrogen fixation in root nodules of soybean plants (Glycine max) grown under flooded conditions. Plant Prod Sci 5:294–300. https://doi.org/10.1626/pps.5.294
Shimamura S, Mochizuki T, Nada Y, Fukuyama M (2003) Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean (Glycine max) under flooded conditions. Plant Soil 251:351–359. https://doi.org/10.1023/A:1023036720537
Shimamura S, Yamamoto R, Nakamura T, Shimada S, Komatsu S (2010) Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Ann Bot 106:277–284. https://doi.org/10.1093/aob/mcq123
Sidhu GK, Tuan PA, Renault S, Daayf F, Ayele BT (2020) Polyamine-Mediated Transcriptional Regulation of Enzymatic Antioxidative Response to Excess Soil Moisture during Early Seedling Growth in Soybean. Biology 9:185. https://doi.org/10.3390/biology9080185
Singh G (2010) The soybean: botany, production and uses. CAB International, Wallingford
Sprent JI (1969) Prolonged reduction of acetylene by detached soybean nodules. Planta 88:372–375. https://doi.org/10.1007/BF00387466
Striker GG (2012) Flooding stress on plants: anatomical, morphological and physiological responses. In: Kiogora, J. (Ed). Botany. InTech. pp 3–28
Sung FJM (1993) Waterlogging effect on nodule nitrogenase and leaf nitrate reductase activities in soybean. Field Crops Res 35:183–189. https://doi.org/10.1016/0378-4290(93)90152-D
Takahashi H, Xiaohua Q, Shimamura S, Yanagawa A, Hiraga S, Nakazono M (2018) Sucrose supply from leaves is required for aerenchymatous phellem formation in hypocotyl of soybean under waterlogged conditions. Ann Bot 121:723–732. https://doi.org/10.1093/aob/mcx205
Thomas AL, Guerreiro SMC, Sodek L (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Ann Bot 96:1191–1198. https://doi.org/10.1093/aob/mci272
Valliyodan B, Ye H, Song L, Murphy M, Shannon JG, Nguyen HT (2017) Genetic diversity and genomic strategies for improving drought and waterlogging tolerance in soybeans. J Exp Bot 68:1835–1849. https://doi.org/10.1093/jxb/erw433
Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390. https://doi.org/10.1146/annurev.pp.42.060191.002105
Voesenek LACJ, Sasidharan R (2013) Ethylene–and oxygen signalling–drive plant survival during flooding. Plant Biol 15:426–435. https://doi.org/10.1111/plb.12014
Walker BA, Pate JS, Kuo J (1983) Nitrogen fixation by nodulated roots of Viminaria juncea (Schrad. & Wendl.) Hoffmans, (Fabaceae) when submerged in water. Funct Plant Biol 10:409–421. https://doi.org/10.1071/PP9830409
Wu C, Mozzoni LA, Moseley D, Hummer W, Ye H, Chen P, Nguyen H (2020) Genome-wide association mapping of flooding tolerance in soybean. Mol Breed 40:1–14. https://doi.org/10.1007/s11032-019-1086-0
Yamane K, Iijima M (2016) Nodulation control of crack fertilization technique reduced the growth inhibition of soybean caused by short-term waterlogging at early vegetative stage. Plant Prod Sci 19:438–448. https://doi.org/10.1080/1343943X.2016.1164573
Yamauchi T, Shimamura S, Nakazono M, Mochizuki T (2013) Aerenchyma formation in crop species: a review. Field Crops Res 152:8–16. https://doi.org/10.1016/j.fcr.2012.12.008
Ye H, Song L, Chen H, Valliyodan B, Cheng P, Ali L, Nguyen HT (2018) A major natural genetic variation associated with root system architecture and plasticity improves waterlogging tolerance and yield in soybean. Plant Cell Environ 41:2169–2182. https://doi.org/10.1111/pce.13190
Funding
RP has a postdoctoral fellowship from CONICET (Argentina).
Author information
Authors and Affiliations
Contributions
RP made the database. RP, DM and GS wrote the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
All the authors give their consent to participate.
Consent for publication
All the authors give their consent for publication.
Conflicts of interest
The authors have no conflict of interest.
Additional information
Responsible Editor: Al Imran Malik.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 325 kb)
Rights and permissions
About this article
Cite this article
Ploschuk, R.A., Miralles, D.J. & Striker, G.G. A quantitative review of soybean responses to waterlogging: agronomical, morpho-physiological and anatomical traits of tolerance. Plant Soil 475, 237–252 (2022). https://doi.org/10.1007/s11104-022-05364-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05364-x