Abstract
Background and aims
Forage legumes form mutualistic interactions with specialized soil rhizobia bacteria that inhabit root nodules and fix atmospheric nitrogen. However, legumes are sensitive to drought stress, which can interrupt nodulation and symbiotic nitrogen fixation (SNF). We hypothesize that drought-impaired SNF may influence soil nitrogen availability and soil microbial diversity.
Methods
Here, we evaluated the effects of drought on nodulation, plant growth, physiological parameters, SNF, soil nitrogen availability, soil extracellular enzyme activity, and soil microbiome of alfalfa (Medicago sativa) and red clover (Trifolium pratense). The drought treatments were imposed at the flowering stage by maintaining soil moisture contents at 20% field capacity (FC) (severe drought), 40% FC (moderate drought), and 80% FC (well-watered) for three weeks.
Results
Drought significantly reduced nodulation, root and shoot growth, and SNF in alfalfa and red clover. Soil available nitrogen was significantly increased following severe drought conditions. The enzyme assays showed reduced activity of N-acetyl-glucosaminidase and β-D cellobiosidase enzymes under drought stress in alfalfa and red clover, respectively. Microbiome data showed shifts in the relative abundance of some key bacterial taxa under drought stress.
Conclusion
Overall results indicate that drought has deleterious effects on SNF and plant growth, affecting carbon and nitrogen cycling enzymes, soil nitrogen availability, and soil microbial diversity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data pertinent to this work are included in the article and the Supplementary files.
References
Acosta-Martínez V, Cotton J, Gardner T, Moore-Kucera J, Zak J, Wester D, Cox S (2014) Predominant bacterial and fungal assemblages in agricultural soils during a record drought/heat wave and linkages to enzyme activities of biogeochemical cycling. Appl Soil Ecol 84:69–82. https://doi.org/10.1016/j.apsoil.2014.06.005
Ashraf M, O’Leary JW (1996) Effect of drought stress on growth, water relations, and gas exchange of two lines of sunflower differing in degree of salt tolerance. Int J Plant Sci 157:729–732. https://doi.org/10.1086/297395
Bachar A, Al-Ashhab A, Soares MIM, Sklarz MY, Angel R, Ungar ED, Gillor O (2010) Soil microbial abundance and diversity along a low precipitation gradient. Microb Ecol 60:453–461. https://doi.org/10.1007/S00248-010-9727-1
Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241. https://doi.org/10.1038/ISMEJ.2013.104
Basak R, Wahid KA, Dinh A, Soolanayakanahally R, Fotouhi R, Mehr AS (2020) Rapid and efficient determination of relative water contents of crop leaves using electrical impedance spectroscopy in vegetative growth stage. Remote Sens 12:1753. https://doi.org/10.3390/rs12111753
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, KÓ§rner C, de Boeck H, Christensen JH, Leuzinger S, Janssens IA et al (2012) Precipitation manipulation experiments–challenges and recommendations for the future. Ecol Lett 15:899–911. https://doi.org/10.1111/j.1461-0248.2012.01793.x
Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148. https://doi.org/10.3389/fmicb.2014.00148
Berg G, Rybakova D, Grube M, Köberl M (2016) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002. https://doi.org/10.1093/jxb/erv466
Bogati K, Walczak M (2022) The impact of drought stress on soil microbial community, enzyme activities and plants. Agron 12:1–26. https://doi.org/10.3390/agronomy12010189
Bouskill NJ, Wood TE, Baran R, Ye Z, Bowen BP, Lim HC, Zhou J, Van Nostrand JD, Nico P, Northen TR et al (2016) Belowground response to drought in a tropical forest soil. I. changes in microbial functional potential and metabolism. Front Microbiol 7:525. https://doi.org/10.3389/fmicb.2016.00525
Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427. https://doi.org/10.1016/0038-0717(82)90099-2
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Cameron KC, Di HJ, Moir JL (2013) Nitrogen losses from the soil/plant system: a review. Ann Appl Biol 162:145–173. https://doi.org/10.1111/aab.12014
Cavaglieri L, Orlando J, Etcheverry M (2009) Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiol Res 164:391–399. https://doi.org/10.1016/j.micres.2007.03.006
Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with Soil Microbial functions. PLoS ONE 8:e55731. https://doi.org/10.1371/journal.pone.0055731
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196
Chong J, Liu P, Zhou G, Xia J (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc 15:799–821. https://doi.org/10.1038/s41596-019-0264-1
Christie BR, Bennett RJ (1984) OAC Minto Alfafla. Can J Plant Sci 64:419–421
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acid Res 42:D633–D642. https://doi.org/10.1093/nar/gkt1244
de Freitas IC, Ferreira EA, Alves MA, de Oliveira JC, Frazão LA (2023) Growth, nodulation, production, and physiology of leguminous plants in integrated production systems. Agrosyst Geosci Environ 6:e20343. https://doi.org/10.1002/agg2.20343
De Haan RL, Schuiteman MA, Vos RJ (2017) Residual soil nitrate content and profitability of five cropping systems in northwest Iowa. PLoS ONE 12:e0171994. https://doi.org/10.1371/journal.pone.0171994
De Vries FT, Wallenstein MD (2017) Below-ground connections underlying above-ground food production: a framework for optimising ecological connections in the rhizosphere. J Ecol 105:913–920. https://doi.org/10.1111/1365-2745.12783
De Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274
del Castillo LD, Hunt S, Layzell DB (1994) The role of oxygen in the regulation of nitrogenase activity in drought-stressed soybean nodules. Plant Physiol 106:949–955
Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327. https://doi.org/10.1111/j.1574-6941.2010.00860.x
Dey R, Lewis SC, Arblaster JM, Abram NJ (2019) A review of past and projected changes in Australia’s rainfall. Wiley Interdiscip Rev Clim Change 10:e00577. https://doi.org/10.1002/wcc.577
Enebe MC, Babalola OO (2018) The influence of plant growth-promoting rhizobacteria in plant tolerance to abiotic stress: a survival strategy. Appl Microbiol Biotech 102:7821–7835. https://doi.org/10.1007/s00253-018-9214-z
Fageria NK (2014) Nitrogen harvest index and its association with crop yields. J Plant Nutr 37:795–810. https://doi.org/10.1080/01904167.2014.881855
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2017) Drought stress in grain legumes during reproduction and grain filling. J Agro Crop Sci 203:81–102. https://doi.org/10.1111/jac.12169
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. https://doi.org/10.1051/agro:2008021
Fernández-Luqueño F, Dendooven L, Munive A, Corlay-Chee L, Serrano-Covarrubias LM, Espinosa-Victoria D (2008) Micro-morphology of common bean (Phaseolus vulgaris L.) nodules undergoing senescence. Acta Physiol Plant 30:545–552. https://doi.org/10.1007/s11738-008-0153-7
Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176. https://doi.org/10.1016/s0038-0717(02)00251-1
Finkel OM, Castrillo G, Paredes SH, González IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163. https://doi.org/10.1016/j.pbi.2017.04.018
Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ (2018) Assembly and ecological function of the root microbiome across angiosperm plant species. PNAS 115:E1157–E1165. https://doi.org/10.1073/pnas.1717617115
Fustec J, Lesuffleur F, Mahieu S, Cliquet JB (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572
Geisseler D, Horwath WR, Scow KM (2011) Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity. Pedobiologia (Jena) 54:71–78. https://doi.org/10.1016/j.pedobi.2010.10.001
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397. https://doi.org/10.1016/j.soilbio.2011.03.017
González EM, Larrainzar E, Marino D, Wienkoop S, Gil-Quintana E, Arrese-Igor C (2015) Physiological responses of N2-fixing legumes to water limitation. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in a changing environment. Springer International Publishing, pp 5–33. https://doi.org/10.1007/978-3-319-06212-9_2
Hartman K, Tringe SG (2019) Interactions between plants and soil shaping the root microbiome under abiotic stress. Biochem J 476:2705–2724. https://doi.org/10.1042/BCJ20180615
Herrmann L, Chotte JL, Thuita M, Lesueur D (2014) Effects of cropping systems, maize residues application and N fertilization on promiscuous soybean yields and diversity of native rhizobia in Central Kenya. Pedobiologia (Jena) 57:75–85. https://doi.org/10.1016/j.pedobi.2013.12.004
Hewins DB, Fatemi F, Adams B, Carlyle C, Chang SX, Bork EW (2015) Grazing, regional climate and soil biophysical impacts on microbial enzyme activity in grassland soil of Western Canada. Pedobiologia (Jena) 58:201–209. https://doi.org/10.1016/j.pedobi.2015.10.003
Hopkins A, Del Prado A (2007) Implications of climate change for grassland in Europe: impacts, adaptations and mitigation options: a review. Grass Forage Sci 62:118–126. https://doi.org/10.1111/j.1365-2494.2007.00575.x
Huber KJ, Vieira S, Sikorski J, Wüst PK, Fösel BU, Gröngröft A, Overmann J (2022) Differential response of acidobacteria to water content, soil type, and land use during an extended drought in African savannah soils. Front Microbiol 13:750456. https://doi.org/10.3389/FMICB.2022.750456/FULL
Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Aust J Plant Physiol 13:803–816
Jacques C, Girodet S, Leroy F, Pluchon S, Salon C, Prudent M (2022) Memory acclimation of water stress in pea rely on root system’s plasticity and plant’s ionome modulation. Front Plant Sci 13:1089720. https://doi.org/10.3389/fpls.2022.1089720
Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105
Johnson DW, Dijkstra FA, Cheng W (2007) The effects of Glycine max and Helianthus annuus on nutrient availability in two soils. Soil Biol Biochem 39:2160–2163. https://doi.org/10.1016/j.soilbio.2007.01.036
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33. https://doi.org/10.1007/s11104-009-9925-0
Kabiri V, Raiesi F, Ghazavi MA (2016) Tillage effects on soil microbial biomass, SOM mineralization and enzyme activity in a semi-arid calcixerepts. Agric Ecosyst Environ 232:73–84. https://doi.org/10.1016/j.agee.2016.07.022
Kaler AS, Bazzer SK, Sanz-Saez A, Ray JD, Fritschi FB, Purcell LC (2018) Carbon isotope ratio fractionation among plant tissues of soybean. Plant Phenome J 1:1–6. https://doi.org/10.2135/tppj2018.04.0002
Kang Y, Han Y, Torres-Jerez I, Wang M, Tang Y, Monteros M, Udvardi M (2011) System responses to long-term drought and re-watering of two contrasting alfalfa varieties. Plant J 68:871–889. https://doi.org/10.1111/j.1365-313X.2011.04738.x
Kanté M, Riah-Anglet W, Cliquet JB, Trinsoutrot-Gattin I (2021) Soil enzyme activity and stoichiometry: linking soil microorganism resource requirement and legume carbon rhizodeposition. Agron 11:2131. https://doi.org/10.3390/agronomy11112131
Kaspar TC, Taylor HM, Shibles RM (1984) Taproot-elongation rates of soybean cultivars in the glasshouse and their relation to field rooting depth. Crop Sci 24:916–920. https://doi.org/10.2135/cropsci1984.0011183x002400050021x
Kasper S, Christoffersen B, Soti P, Racelis A (2019) Abiotic and biotic limitations to nodulation by leguminous cover crops in south Texas. Agric 9:209. https://doi.org/10.3390/agriculture9100209
Kaushal M, Wani SP (2016) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66:35–42. https://doi.org/10.1007/s13213-015-1112-3
Kavamura NV, Taketani RG, Lançoni MD, Andreote FD, Mendes R, de Melo SI (2013) Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome. PLoS ONE 8:e73606. https://doi.org/10.1371/journal.pone.0073606
Khan N, Bano A (2019) Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 14:e0222302. https://doi.org/10.1371/journal.pone.0222302
Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth MG, Bi K, TerAvest D, Weebadde P, Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth MG, Bi K, TerAvest D, Weebadde P, Kramer DM (2016) MultispeQ beta: a tool for large-scale plant phenotyping connected to the open photosynQ network. R Soc Open Sci 3:160592. https://doi.org/10.1098/rsos.160592
Kunert KJ, Vorster BJ, Fenta BA, Kibido T, Dionisio G, Foyer CH (2016) Drought stress responses in soybean roots and nodules. Front Plant Sci 7:1015. https://doi.org/10.3389/fpls.2016.01015
Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium Genus. Microbiol Res 169:2–17. https://doi.org/10.1016/j.micres.2013.09.012
Lau JA, Lennon JT, Kellogg WK, Karl DM (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109:14058–14062. https://doi.org/10.1073/pnas.1202319109
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87. https://doi.org/10.1038/NATURE16467
Lesuffleur F, Paynel F, Bataillé MP, Le Deunff E, Cliquet JB (2007) Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant Soil 294:235–246. https://doi.org/10.1007/s11104-007-9249-x
Lewin GR, Carlos C, Chevrette MG, Horn HA, McDonald BR, Stankey RJ, Fox BG, Currie CR (2016) Evolution and ecology of Actinobacteria and their bioenergy applications. Annu Rev Microbiol 70:235–254. https://doi.org/10.1146/annurev-micro-102215-095748
Liu F, Jensen CR, Andersen MN (2005) A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Aust J Agric Res 56:1245–1252. https://doi.org/10.1071/AR05062
Liyanage DK, Chathuranga I, Mori BA, Thilakarathna MS (2022) A simple, semi- automated, gravimetric method to simulate drought stress on plants. Agronomy 12:349. https://doi.org/10.3390/agronomy12020349
Liyanage DK, Torkamaneh D, Belzile F, Balasubramanian P, Hill B, Thilakarathna MS (2023) The genotypic variability among short-season soybean cultivars for nitrogen fixation under drought stress. Plants 12:1004. https://doi.org/10.3390/plants12051004
Lumactud RA, Dollete D, Liyanage DK, Szczyglowski K, Hill B, Thilakarathna MS (2023) The effect of drought stress on nodulation, plant growth, and nitrogen fixation in soybean during early plant growth. J Agron Crop Sci 209:345–354. https://doi.org/10.1111/jac.12627
Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, García-Gómez M, Gallardo A, Ulrich W, Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, García-Gómez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitán J, Gutiérrez JR, Huber-Sannwald E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang D, Woods NN, Yuan X, Zaady E, Singh BK (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands. PNAS 112:15684–15689. https://doi.org/10.1073/pnas.1516684112
Mak M, Babla M, Xu SC, O’Carrigan A, Liu XH, Gong YM, Holford P, Chen ZH (2014) Leaf mesophyll K+, H+ and Ca2+ fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean. Environ Exp Bot 98:1–12. https://doi.org/10.1016/j.envexpbot.2013.10.003
Manavalan LP, Guttikonda SK, Phan Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276. https://doi.org/10.1093/pcp/pcp082
Marchin RM, Ossola A, Leishman MR, Ellsworth DS (2020) A simple method for simulating drought effects on plants. Front Plant Sci 10:1715. https://doi.org/10.3389/fpls.2019.01715
Marquez-Garcia B, Shaw D, Cooper JW, Karpinska B, Quain MD, Makgopa EM, Kunert K, Foyer CH (2015) Redox markers for drought-induced nodule senescence, a process occurring after drought-induced senescence of the lowest leaves in soybean (Glycine max). Ann Bot 116:497–510. https://doi.org/10.1093/aob/mcv030
McPherson MR, Wang P, Marsh EL, Mitchell RB, Schachtman DP (2018) Isolation and analysis of microbial communities in soil, rhizosphere, and roots in perennial grass experiments. J Vis Exp 137:e57932. https://doi.org/10.3791/57932
Micheletto S, Rodriguez-Uribe L, Hernandez R, Richins RD, Curry J, O’Connell MA (2007) Comparative transcript profiling in roots of Phaseolus acutifolius and P. Vulgaris under water deficit stress. Plant Sci 173:510–520. https://doi.org/10.1016/j.plantsci.2007.08.003
Miransari M, Riahi H, Eftekhar F, Minaie A, Smith DL (2013) Improving soybean (Glycine max L.) N2 fixation under stress. J Plant Growth Regul 32:909–921. https://doi.org/10.1007/s00344013-9335-7
Moghaddam A, Raza A, Vollmann J, Ardakani MR, Wanek W, Gollner G, Friedel JK (2013) Carbon isotope discrimination and water use efficiency relationships of alfalfa genotypes under irrigated and rain-fed organic farming. Eur J Agron 50:82–89. https://doi.org/10.1016/j.eja.2013.05.010
Mouradi M, Bouizgaren A, Farissi M, Makoudi B, Kabbadj A, Very AA, Sentenac H, Qaddoury A, Ghoulam C (2016) Osmopriming improves seeds germination, growth, antioxidant responses and membrane stability during early stage of Moroccan alfalfa populations under water deficit. Chil J Agric Res 76:265–272. https://doi.org/10.4067/S0718-58392016000300002
Mwale SE, Ochwo-Ssemakula M, Sadik K, Achola E, Okul V, Gibson P, Edema R, Singini W, Rubaihayo P (2017) Response of cowpea genotypes to drought stress in Uganda. Am J Plant Sci 8:720–733. https://doi.org/10.4236/ajps.2017.84050
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48. https://doi.org/10.1111/j.1469-8137.2008.02751.x
Naya L, Ladrera R, Ramos J, González EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 144:1104–1114. https://doi.org/10.1104/pp.107.099648
Naylor D, Coleman-Derr D (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8:2223. https://doi.org/10.3389/fpls.2017.02223
Nishida H, Suzaki T (2018) Nitrate-mediated control of root nodule symbiosis. Curr Opin Plant Biol 44:129–136. https://doi.org/10.1016/j.pbi.2018.04.006
Niu X, Song L, Xiao Y, Ge W (2018) Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid and their potential in alleviating drought stress. Front Microbiol 8:2580. https://doi.org/10.3389/fmicb.2017.02580
Parida AK, Dagaonkar VS, Phalak MS, Umalkar GV, Aurangabadkar LP (2007) Alterations in photosynthetic pigments, protein and osmotic components in cotton genotypes subjected to short-term drought stress followed by recovery. Plant Biotechnol Rep 1:37–48. https://doi.org/10.1007/s11816-006-0004-1
Paynel F, Lesuffleur F, Bigot J, Diquélou S, Cliquet JB (2008) A study of 15N transfer between legumes and grasses. Agron Sustain Dev 28:281–290. https://doi.org/10.1051/agro:2007061
Pohlert T (2022) PMCMRplus: calculate pairwise multiple comparisons of mean rank sums extended. R package version 1.9.6. https://CRAN.R-project.org/package=PMCMRplus. Accessed 20 Aug 2022
Poorter H, Fiorani F, Stitt M, Schurr U, Finck A, Gibon Y, Usadel B, Munns R, Atkin OK, Tardieu F, Pons TL (2012) The art of growing plants for experimental purposes: a practical guide for the plant biologist. Funct Plant Biol 39:821–838. https://doi.org/10.1071/FP12028
Preece C, Peñuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–7. https://doi.org/10.1007/s11104-016-3090-z
Preece C, Verbruggen E, Liu L, Weedon JT, Peñuelas J (2019) Effects of past and current drought on the composition and diversity of soil microbial communities. Soil Biol Biochem 131:28–39. https://doi.org/10.1016/j.soilbio.2018.12.022
R Core Team (2023) R: A language and environment for tatistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 15 Mar 2023
Raeini-Sarjaz M, Barthakur NN, Arnold NP, Jones PJH (1998) Water stress, water use efficiency, carbon isotope discrimination and leaf gas exchange relationships of the bush bean. J Agron Crop Sci 180:173–179. https://doi.org/10.1111/j.1439-037x.1998.tb00387.x
Rehman A, Nautiyal CS (2002) Effect of drought on the growth and survival of the stress-tolerant bacterium Rhizobium sp. NBRI2505 sesbania and its drought-sensitive transposon Tn5 mutant. Curr Microbiol 45:368–377. https://doi.org/10.1007/s00284-002-3770-1
Ren C, Zhao F, Shi Z, Chen J, Han X, Yang G, Feng Y, Ren G (2017) Differential responses of soil microbial biomass and carbon-degrading enzyme activities to altered precipitation. Soil Biol Biochem 115:1–10. https://doi.org/10.1016/j.soilbio.2017.08.002
Rochon JJ, Doyle CJ, Greef JM, Hopkins A, Molle G, Sitzia M, Scholefield D, Smith CJ (2004) Grazing legumes in Europe: a review of their status, management, benefits, research needs and future prospects. Grass Forage Sci 59:197–214
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584/FIG-7
Rouached A, Slama I, Zorrig W, Jdey A, Cukier C, Rabhi M, Talbi O, Limami AM, Abdelly C (2013) Differential performance of two forage species, Medicago truncatula and sulla carnosa, under water-deficit stress and recovery. Crop Pasture Sci 64:254–264. https://doi.org/10.1071/CP13049
Rubiales D, Mikic A (2015) Introduction: legumes in sustainable agriculture. CRC Crit Rev Plant Sci 34:2–3. https://doi.org/10.1080/07352689.2014.897896
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Santos-Medellín C, Liechty Z, Edwards J, Nguyen B, Huang B, Weimer BC, Sundaresan V (2021) Prolonged drought imparts lasting compositional changes to the rice root microbiome. Nat Plants 7:1065–1077. https://doi.org/10.1038/s41477-021-00967-1
Schimel JP (2018) Life in Dry soils: effects of drought on soil microbial communities and processes. Annu Rev Ecol Evol Syst 49:409–432. https://doi.org/10.1146/annurev-ecolsys-110617-062614
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Schwalm CR, Anderegg WRL, Michalak AM, Fisher JB, Biondi F, Koch G, Litvak M, Ogle K, Shaw JD, Wolf A, Schwalm CR, Anderegg WRL, Michalak AM, Fisher JB, Biondi F, Koch G, Litvak M, Ogle K, Shaw JD, Wolf A, Huntzinger DN, Schaefer K, Cook R, Wei Y, Fang Y, Hayes D, Huang M, Jain A, Tian H (2017) Global patterns of drought recovery. Nature 548:202–205. https://doi.org/10.1038/nature23021
Serraj R (2003) Effects of drought stress on legume symbiotic nitrogen fixation: physiological mechanisms. Indian J Exp Biol 41:1136–1141
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155. https://doi.org/10.1093/jxb/50.331.143
Serraj R, Vadez V, Sinclair T, Sinclair TR (2001) Feedback regulation of symbiotic N2 fixation under drought stress. Agron 21:6–7. https://doi.org/10.1051/agro:2001153ï
Steinauer K, Tilman D, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N (2015) Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecol 96:99–112. https://doi.org/10.1890/14-0088.1
Thilakarathna MS, Cope KR (2021) Split-root assays for studying legume-rhizobia symbioses, rhizodeposition, and belowground nitrogen transfer in legumes. J Exp Bot 72:5285–5299. https://doi.org/10.1093/jxb/erab198
Thilakarathna MS, McElroy MS, Chapagain T, Papadopoulos YA, Raizada MN (2016) Belowground nitrogen transfer from legumes to non-legumes under managed herbaceous cropping systems. A review. Agron Sustain Dev 36:58. https://doi.org/10.1007/s13593-016-0396-4
Thilakarathna MS, Moroz N, Raizada MN (2017) A biosensor-based leaf punch assay for glutamine correlates to symbiotic nitrogen fixation measurements in legumes to permit rapid screening of rhizobia inoculants under control conditions. Front Plant Sci 08:1714. https://doi.org/10.3389/fpls.2017.01714
Thilakarathna MS, Raizada MN (2017) A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions. Soil Biol Biochem 105:177–196. https://doi.org/10.1016/j.soilbio.2016.11.022
Thilakarathna MS, Raizada MN (2018) Visualizing glutamine accumulation in root systems involved in the legume–rhizobia symbiosis by placement on agar embedded with companion biosensor cells. Phytobiomes J 2:117–128. https://doi.org/10.1094/PBIOMES-07-18-0031-TA
Thilakarathna MS, Raizada MN (2019) A biosensor-based assay (GlnLux-Agar) shows defoliation triggers rapid release of glutamine from nodules and young roots of forage leguumes. Phytobiomes J 3:85–91. https://doi.org/10.1094/PBIOMES-03-19-0014-Rs
Tóth Z, Táncsics A, Kriszt B, Kröel-Dulay G, Ónodi G, Hornung E (2017) Extreme effects of drought on composition of the soil bacterial community and decomposition of plant tissue. Eur J Soil Sci 68:504–513. https://doi.org/10.1111/ejss.12429
Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2008) Hydrolytic enzyme activities in agricultural and forest soils. Some implications for their use as indicators of soil quality. Soil Biol Biochem 40:2146–2155. https://doi.org/10.1016/j.soilbio.2008.03.015
Udvardi M, Poole PS (2013) Transport and metabolism in lgume rhizobia symbioses. Annu Rev Plant Biol 64:781–805. https://doi.org/10.1146/annurev-arplant
Valentine AJ, Benedito VA, Kang Y (2011) Legume nitrogen fixation and soil abiotic stress: from physiology to genomics and beyond. In: Foyer CH, Zhang H (eds) Nitrogen metabolism in plants in the post-genomic era, vol 42, Wiley-Blackwell Publishing, pp 207–248. https://doi.org/10.1002/9781444328608.ch9
Vaseva I, Akiscan Y, Demirevska K, Anders I, Feller U (2011) Drought stress tolerance of red and white clover-comparative analysis of some chaperonins and dehydrins. Sci Hortic 130:653–659. https://doi.org/10.1016/j.scienta.2011.08.021
Wang W, Wang C, Pan D, Zhang Y, Luo B, Ji J (2018) Effects of drought stress on photosynthesis and chlorophyll fluorescence images of soybean (Glycine max) seedlings. Int J Agric Biol Eng 11:196–201. https://doi.org/10.25165/j.ijabe.20181102.3390
Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Qi, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056. https://doi.org/10.1128/AEM.02294-08
Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. https://doi.org/10.1186/s40168-017-0237-y
Wichern F, Eberhardt E, Mayer J, Joergensen RG, Müller T (2008) Nitrogen rhizodeposition in agricultural crops: methods, estimates and future prospects. Soil Biol Biochem 40:30–48. https://doi.org/10.1016/j.soilbio.2007.08.010
Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, Kim YM, Zink EM, Engbrecht KM, Wang Y, Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, Kim Y-M, Zink EM, Engbrecht KM, Wang Yi, Gao C, DeGraaf S, Madera MA, Sievert JA, Hollingsworth J, Birdseye D, Scheller HV, Hutmacher R, Dahlberg J, Jansson C, Taylor JW, Lemaux PG, Coleman-Derr D (2018) Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. PNAS 115:E4284–E4293. https://doi.org/10.1073/PNAS.1717308115
Yuste JC, Fernandez-Gonzales AJ, Fernandez-Lopez M, Ogaya R, Penuelas J, Sardans J, Lloret F (2014) Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation. Soil Biol Biochem 69:223–233. https://doi.org/10.1016/j.soilbio.2013.10.045
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989. https://doi.org/10.1128/mmbr.63.4.968-989.1999
Zargar SM, Gupta N, Nazir M, Mahajan R, Malik FA, Sofi NR, Shikari AB, Salgotra RK (2017) Impact of drought on photosynthesis: molecular perspective. Plant Gene 11:154–159. https://doi.org/10.1016/j.plgene.2017.04.003
Zhang C, Shi S, Liu Z, Yang F, Yin G (2018) Drought tolerance in alfalfa (Medicago sativa L.) varieties is associated with enhanced antioxidative protection and declined lipid peroxidation. J Plant Physiol 232:226–240. https://doi.org/10.1016/j.jplph.2018.10.023
Acknowledgements
Thanks to the Department of Science and Technology of the Republic of the Philippines for providing graduate students with scholarship opportunities such as the DOST-SEI UAlberta S&T Graduate Scholarship.
Funding
This research was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (RGPIN-2020-04425) to MST.
Author information
Authors and Affiliations
Contributions
MST, DD, and CC conceptualized and designed the research. DD performed the experiments and collected data. MST, CC and KS provided resources. DD, RAL and BH performed formal data analysis. DD and RAL performed the data analysis and visualization. DD wrote the original draft. All the authors contributed to the review and editing of the manuscript. MST acquired the funding.
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Responsible Editor: Euan K. James.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 2.53)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dollete, D., Lumactud, R.A., Carlyle, C.N. et al. Effect of drought stress on symbiotic nitrogen fixation, soil nitrogen availability and soil microbial diversity in forage legumes. Plant Soil 495, 445–467 (2024). https://doi.org/10.1007/s11104-023-06348-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06348-1