Enhancing stress resilience in soybeans (Glycine max): assessing the efficacy of priming and cross-priming for mitigating water deficit and waterlogging effects
Adriano U. Bester A B * , Eduardo P. Shimoia A , Cristiane J. Da-Silva A C * , Douglas A. Posso A , Ivan R. Carvalho D , Fernanda M. Corrêa A , Ana C. B. de Oliveira E and Luciano do Amarante AA
B
C
D
E
Handling Editor: Manuela Chaves
Abstract
Priming enables plants to respond more promptly, minimise damage, and survive subsequent stress events. Here, we aimed to assess the efficacy of priming and cross-priming in mitigating the stress caused by waterlogging and/or dehydration in soybeans (Glycine max). Soybean plants were cultivated in a greenhouse in plastic pots in which soil moisture was maintained at pot capacity through irrigation. The first stress was applied in plants at the vegetative stage for 5 days and involved either dehydration or waterlogging, depending on the treatment. Subsequently, the plants were irrigated or drained and maintained at pot capacity until the second stress. For the second stress, the conditions were repeated in plants at the reproductive stage. We then evaluated the levels of hydrogen peroxide (H2O2), lipid peroxidation, total soluble sugars (TSS), amino acids, proline, and starch, and the activity of antioxidant, fermentative, and aminotransferase enzymes. Under waterlogging and dehydration, priming and cross-priming significantly increased the activity of antioxidant enzymes and the levels of TSS, amino acids, and proline while reducing H2O2 concentration and lipid peroxidation. Under waterlogging, priming suppressed fermentative activity and increased carbohydrate content. This demonstrates that soybean plants activate their defence systems more promptly when subjected to priming.
Keywords: abiotic stress, antioxidant defence, drought, fermentation, flooding, hypoxia, osmolytes, oxidative stress, water stress.
References
Agualongo DAP, Da-Silva CJ, Garcia N, et al. (2022) Waterlogging priming alleviates the oxidative damage, carbohydrate consumption, and yield loss in soybean (Glycine max) plants exposed to waterlogging. Functional Plant Biology 49, 1029-1042.
| Crossref | Google Scholar | PubMed |
Ahanger MA, Ashraf M, Bajguz A, et al. (2018) Brassinosteroids regulate growth in plants under stressful environments and crosstalk with other potential phytohormones. Journal of Plant Growth Regulation 37, 1007-1024.
| Crossref | Google Scholar |
Azevedo RA, Alas RM, Smith RJ, et al. (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiologia Plantarum 104, 280-292.
| Crossref | Google Scholar |
Bandeppa S, Chandra P, Santosh S, et al. (2022) Plant growth-promoting microorganism-mediated abiotic stress resilience in crop plants. In ‘Trends of applied microbiology for sustainable economy’. Developments in Applied Microbiology and Biotechnology. (Eds R Soni, DC Suyal, AN Yadav, R Goel) pp. 395–419. (Academic Press)
Bester AU, Shimoia EP, Da-Silva CJ, et al. (2024) Physiological mechanisms of cross-stress and memory in soybean plants subjected to water deficit and waterlogging. Environmental and Experimental Botany 222, 105749.
| Crossref | Google Scholar |
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Analytical Biochemistry 17, 278-293.
| Crossref | Google Scholar | PubMed |
Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology 116, 651-658.
| Crossref | Google Scholar | PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar | PubMed |
Bui LT, Novi G, Lombardi L, et al. (2019) Conservation of ethanol fermentation and its regulation in land plants. Journal of Experimental Botany 70, 1815-1827.
| Crossref | Google Scholar | PubMed |
da-Silva CJ, do Amarante L (2020) Short-term nitrate supply decreases fermentation and oxidative stress caused by waterlogging in soybean plants. Environmental and Experimental Botany 176, 104078.
| Crossref | Google Scholar |
Dumanović J, Nepovimova E, Natić M, et al. (2021) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Frontiers in Plant Science 11, 552969.
| Crossref | Google Scholar |
Garcia N, da-Silva CJ, Cocco KLT, et al. (2020) Waterlogging tolerance of five soybean genotypes through different physiological and biochemical mechanisms. Environmental and Experimental Botany 172, 103975.
| Crossref | Google Scholar |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309-314.
| Crossref | Google Scholar | PubMed |
Good AG, Muench DG (1992) Purification and characterization of an anaerobically induced alanine aminotransferase from barley roots. Plant Physiology 99, 1520-1525.
| Crossref | Google Scholar | PubMed |
Graham D, Smydzuk J (1965) Use of anthrone in the quantitative determination of hexose phosphates. Analytical Biochemistry 11, 246-255.
| Crossref | Google Scholar | PubMed |
Gugliuzza G, Talluto G, Martinelli F, et al. (2020) Water deficit affects the growth and leaf metabolite composition of young loquat plants. Plants 9, 274.
| Crossref | Google Scholar | PubMed |
Guo J, Wang H, Liu S, et al. (2022) Parental drought priming enhances tolerance to low temperature in wheat (Triticum aestivum) offspring. Functional Plant Biology 49(11), 946-957.
| Crossref | Google Scholar | PubMed |
Hanson AD, Jacobsen JV, Zwar JA (1984) Regulated expression of three alcohol dehydrogenase genes in barley aleurone layers. Plant Physiology 75, 573-581.
| Crossref | Google Scholar | PubMed |
Haverroth EJ, Da-Silva CJ, Taggart M, Oliveira LA, Cardoso AA (2024) Shoot hydraulic impairments induced by root waterlogging: parallels and contrasts with drought. Plant Physiology kiae336.
| Crossref | Google Scholar |
Hirabayashi Y, Kanae S, Emori S, et al. (2008) Global projections of changing risks of floods and droughts in a changing climate. Hydrological Sciences Journal 53(4), 754-772.
| Crossref | Google Scholar |
Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. California Agricultural Experimental Station 347, 1-32.
| Google Scholar |
Hossain MM, Liu X, Qi X, et al. (2014) Differences between soybean genotypes in physiological response to sequential soil drying and rewetting. The Crop Journal 2(6), 366-380.
| Crossref | Google Scholar |
Lai D, Mao Y, Zhou H, et al. (2014) Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa. Plant Science 225, 117-129.
| Crossref | Google Scholar | PubMed |
Liu S, Li X, Larsen DH, et al. (2017) Drought priming at vegetative growth stage enhances nitrogen-use efficiency under post-anthesis drought and heat stress in wheat. Journal of Agronomy and Crop Science 203, 29-40.
| Crossref | Google Scholar |
Liu H, Able AJ, Able JA (2022) Priming crops for the future: rewiring stress memory. Trends in Plant Science 27, 699-716.
| Crossref | Google Scholar | PubMed |
Mccready RM, Guggolz J, Silviera V, et al. (1950) Determination of starch and amylose in vegetables. Analytical Chemistry 22, 1156-1158.
| Crossref | Google Scholar |
Nakano Y, Asada KH (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867-880.
| Crossref | Google Scholar |
Qian L, Chen X, Wang X, et al. (2020) The effects of flood, drought, and flood followed by drought on yield in cotton. Agronomy 10, 555.
| Crossref | Google Scholar |
Raza A, Razzaq A, Mehmood SS, et al. (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8, 34.
| Crossref | Google Scholar | PubMed |
Rena AB, Masciotti GZ (1976) The effect of dehydration on nitrogen metabolism and growth of bean cultivars (Phaseolus vulgaris L.). Revista Ceres 23, 288-301.
| Google Scholar |
Rocha M, Sodek L, Licausi F, et al. (2010) Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 39, 1043-1053.
| Crossref | Google Scholar | PubMed |
Sheteiwy MS, Shao H, Qi W, et al. (2021) Seed priming and foliar application with jasmonic acid enhance salinity stress tolerance of soybean (Glycine max L.) seedlings. Journal of the Science of Food and Agriculture 101, 2027-2041.
| Crossref | Google Scholar | PubMed |
Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS ONE 7, e38554.
| Crossref | Google Scholar | PubMed |
Tan X, Xu H, Khan S, et al. (2018) Plant water transport and aquaporins in oxygen-deprived environments. Journal of Plant Physiology 227, 20-30.
| Crossref | Google Scholar | PubMed |
Teixeira WF, Soares LH, Fagan EB, et al. (2020) Amino acids as stress reducers in soybean plant growth under different water-deficit conditions. Journal of Plant Growth Regulation 39, 905-919.
| Crossref | Google Scholar |
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 59-66.
| Crossref | Google Scholar |
Wang X, Wu Z, Zhou Q, et al. (2022) Physiological response of soybean plants to water deficit. Frontiers in Plant Science 12, 809692.
| Crossref | Google Scholar | PubMed |
Wang L, Sui Y, Zhang P, et al. (2024) Polystyrene nanoplastics in soil impair drought priming-induced low temperature tolerance in wheat. Plant Physiology and Biochemistry 210, 108643.
| Crossref | Google Scholar |
Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. The Analyst 80, 209-214.
| Crossref | Google Scholar |
Zhou J, Xia X-J, Zhou Y-H, et al. (2014) RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. Journal of Experimental Botany 65, 595-607.
| Crossref | Google Scholar | PubMed |
Zhou W, Chen F, Meng Y, et al. (2020) Plant waterlogging/flooding stress responses: from seed germination to maturation. Plant Physiology and Biochemistry 148, 228-236.
| Crossref | Google Scholar | PubMed |