Abstract
With the changing global climate, drought is considered one of the most devastating abiotic factors. Drought not only limits plant productivity by changing growth and development but also alters the microbiome in the rhizosphere. In addition to influencing the root microbes, drought modifies the root exudate's composition and profile in the rhizosphere. Plant health, root exudation, and abundance of soil microbes in the rhizosphere are inter-connected. The composition of root exudate is altered in terms of the abundance of primary metabolites such as sugar, amino acids, and organic acids and secondary metabolites like flavonoids, strigolactones, and terpenoids. Here, we discuss how a plethora of soil microbes may be involved in a feedback mechanism by utilizing root exudate constituents to promote drought tolerance in plants. Furthermore, plant drought tolerance is positively associated with strigolactones (SLs) exudation via coordination with ABA hormone signaling. Lastly, while the collection, sampling, and analysis of root exudates are all promising, we attempted to present advanced methodology and the development of novel processes in the review, which benefited greatly.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel-Salam E, Alatar A, El-Sheikh MA (2018) Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J Biol Sci 25:1772–1780. https://doi.org/10.1016/j.sjbs.2017.10.015
Abe S, Sado A, Tanaka K et al (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci U S A 111:18084–18089. https://doi.org/10.1073/pnas.1410801111
Adeyemi O, Keshavarz-Afshar R, Jahanzad E et al (2020) Effect of wheat cover crop and split nitrogen application on corn yield and nitrogen use efficiency. Agronomy. https://doi.org/10.3390/agronomy10081081
Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186. https://doi.org/10.1146/annurev-arplant-043014-114759
Allard-Massicotte R, Tessier L, Lécuyer F et al (2016) Bacillus subtilis early colonization of Arabidopsis thaliana roots. Mbio 7:1–10. https://doi.org/10.1128/mBio.01664-16.Invited
Alvi AF, Sehar Z, Fatma M et al (2022) Strigolactone: an emerging growth regulator for developing resilience in plants. Plants 11:2604. https://doi.org/10.3390/plants11192604
Aroca R, Ruiz-Lozano JM, Zamarreño AM et al (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55. https://doi.org/10.1016/j.jplph.2012.08.020
Ashraf M, Akram NA, Al-Qurainy F, Foolad MR (2011) Drought tolerance. roles of organic osmolytes, growth regulators, and mineral nutrients. Adv Agron 111:249–296. https://doi.org/10.1016/B978-0-12-387689-8.00002-3
Aslam M, Maqbool MA, Cengiz R (2015) Drought stress in maize (Zea mays L.). Springer, Cham
Azhar MT, Rehman A (2018) Overview on effects of water stress on cotton plants and productivity. In: Biochemical, physiological and molecular avenues for combating abiotic stress in plants, pp 297–316. https://doi.org/10.1016/B978-0-12-813066-7.00016-4
Badri D, Chaparro JM, Zhang R et al (2013) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512. https://doi.org/10.1074/jbc.M112.433300
Baltruschat H, Fodor J, Harrach BD et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510. https://doi.org/10.1111/j.1469-8137.2008.02583.x
Bastías DA, Johnson LJ, Card SD (2020) Symbiotic bacteria of plant-associated fungi: friends or foes? Curr Opin Plant Biol 56:1–8
Batool T, Ali S, Seleiman MF et al (2020) Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Sci Rep. https://doi.org/10.1038/s41598-020-73489-z
Begum N, Qin C, Ahanger MA et al (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068
Bell CW, Asao S, Calderon F et al (2015) Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth. Soil Biol Biochem 85:170–182. https://doi.org/10.1016/j.soilbio.2015.03.006
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berendsen R, Schlaeppi K (2019) Editorial overview: Environmental microbiology: #PlantMicrobiome. Curr. Opin. Microbiol 49:iii-v. https://doi.org/10.1016/j.mib.2019.11.002
Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci 12:1–18. https://doi.org/10.3389/fpls.2021.615114
Bhattacharyya SS, Furtak K (2023) Soil–plant–microbe interactions determine soil biological fertility by altering rhizospheric nutrient cycling and biocrust formation. Sustainability (switzerland) 15:625
Bista DR, Heckathorn SA, Jayawardena DM et al (2018) Effects of drought on nutrient uptake and the levels of nutrient-uptake proteins in roots of drought-sensitive and -tolerant grasses. Plants. https://doi.org/10.3390/plants7020028
Bruno M, Al-Babili S (2016) On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27. Planta 243:1429–1440. https://doi.org/10.1007/s00425-016-2487-5
Bu Q, Lv T, Shen H et al (2014) Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol 164:424–439. https://doi.org/10.1104/pp.113.226837
Canarini A, Kaiser C, Merchant A et al (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157
Canarini A, Merchant A, Dijkstra FA (2016) Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere 2:85–97. https://doi.org/10.1016/j.rhisph.2016.06.003
Caparas M, Zobel Z, Castanho ADA, Schwalm CR (2021) Increasing risks of crop failure and water scarcity in global breadbaskets by 2030. Environ Res Lett. https://doi.org/10.1088/1748-9326/ac22c1
Chance B, William BR (1955) © 1955 Nature Publishing Group © 1955 Nature Publishing Group. Nature 176:1955
Chen Y, Yao Z, Sun Y et al (2022) Current studies of the effects of drought stress on root exudates and rhizosphere microbiomes of crop plant species. Int J Mol Sci 23:2374
Comas LH, Becker SR, Cruz VM et al (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442
Conesa MR, Conejero W, Vera J et al (2021) Irrigation management practices in nectarine fruit quality at harvest and after cold storage. Agric Water Manag. https://doi.org/10.1016/j.agwat.2020.106519
de Cuyper C, Struk S, Braem L et al (2017) Strigolactones, karrikins and beyond. Plant Cell Environ 40:1691–1703
de la Rosa JM, Conesa MR, Domingo R et al (2016) Combined effects of deficit irrigation and crop level on early nectarine trees. Agric Water Manag 170:120–132. https://doi.org/10.1016/J.AGWAT.2016.01.012
de Vries FT, Brown C, Stevens CJ (2016) Grassland species root response to drought: consequences for soil carbon and nitrogen availability. Plant Soil 409:297–312. https://doi.org/10.1007/s11104-016-2964-4
de Vries FT, Williams A, Stringer F et al (2019a) Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytol 224:132–145. https://doi.org/10.1111/nph.16001
Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol. https://doi.org/10.3389/fmicb.2013.00216
Du H, Huang F, Wu N et al (2018) Integrative regulation of drought escape through ABA-dependent and -independent pathways in rice. Mol Plant 11:584–597. https://doi.org/10.1016/j.molp.2018.01.004
Dunn WB, Erban A, Weber RJM et al (2013) Mass appeal: metabolite identification in mass spectrometry-focused untargeted metabolomics. Metabolomics 9:44–66. https://doi.org/10.1007/s11306-012-0434-4
Egamberdieva D, Wirth SJ, Alqarawi AA et al (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104
Eltigani A, Müller A, Ngwene B, George E (2022) Physiological and morphological responses of okra (Abelmoschus esculentus L.) to rhizoglomus irregulare inoculation under ample water and drought stress conditions are cultivar dependent. Plants. https://doi.org/10.3390/plants11010089
Fahad S, Bajwa AA, Nazir U et al (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147
Faizan M, Faraz A, Sami F et al (2020) Role of strigolactones: signalling and crosstalk with other phytohormones. Open Life Sci 15:217–228
Farooq M, Siddique KHM, Rehman H et al (2011) Rice direct seeding: experiences, challenges and opportunities. Soil Tillage Res 111:87–98
Ferrero M, Pagliarani C, Novák O et al (2018) Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries. J Exp Bot 69:2391–2402. https://doi.org/10.1093/jxb/ery033
Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188. https://doi.org/10.1016/j.apsoil.2008.04.005
Fry EL, Evans AL, Sturrock CJ et al (2018) Root architecture governs plasticity in response to drought. Plant Soil 433:189–200. https://doi.org/10.1007/s11104-018-3824-1
Fuhrer T, Zamboni N (2015) High-throughput discovery metabolomics. Curr Opin Biotechnol 31:73–78. https://doi.org/10.1016/j.copbio.2014.08.006
Gagné-Bourque F, Bertrand A, Claessens A et al (2016) Alleviation of drought stress and metabolic changes in timothy (Phleum pratense L.) colonized with Bacillus subtilis B26. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00584
Galindo A, Collado-González J, Griñán I et al (2018) Deficit irrigation and emerging fruit crops as a strategy to save water in Mediterranean semiarid agrosystems. Agric Water Manag 202:311–324. https://doi.org/10.1016/j.agwat.2017.08.015
Gao J, Sasse J, Lewald KM et al (2018) Ecosystem fabrication (EcoFAB) protocols for the construction of laboratory ecosystems designed to study plant-microbe interactions. J vis Exp 2018:1–16. https://doi.org/10.3791/57170
Gargallo-Garriga A, Preece C, Sardans J et al (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep. https://doi.org/10.1038/s41598-018-30150-0
Ghanbary E, Fathizadeh O, Pazhouhan I et al (2021) Drought and pathogen effects on survival, leaf physiology, oxidative damage, and defense in two middle eastern oak species. Forests 12:1–23. https://doi.org/10.3390/f12020247
Gougoulias C, Clark JM, Shaw LJ (2014) The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems. J Sci Food Agric 94:2362–2371
Gupta A, Gupta R, Singh RL (2017) Microbes and environment. In: Singh RL (ed) Principles and applications of environmental biotechnology for a sustainable future. Springer, Singapore, pp 43–84
Guyonnet JP, Vautrin F, Meiffren G et al (2017) The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fix022
Haase S, Neumann G, Kania A et al (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221. https://doi.org/10.1016/j.soilbio.2007.03.014
Haichar FEZ, Marol C, Berge O et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. https://doi.org/10.1038/ismej.2008.80
Haider I, Andreo-Jimenez B, Bruno M et al (2018) The interaction of strigolactones with abscisic acid during the drought response in rice. J Exp Bot 69:2403–2414. https://doi.org/10.1093/jxb/ery089
Haldar S, Sengupta S (2015) Plant-microbe cross-talk in the rhizosphere: insight and biotechnological potential 9:1-7. doi: 10.2174/1874285801509010001
Haq BUI, Ahmad MZ, Ur Rehman N et al (2017) Functional characterization of soybean strigolactone biosynthesis and signaling genes in Arabidopsis MAX mutants and GmMAX3 in soybean nodulation. BMC Plant Biol. https://doi.org/10.1186/s12870-017-1182-4
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
Hashem A, Kumar A, Al-Dbass AM et al (2019) Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi J Biol Sci 26:614–624. https://doi.org/10.1016/j.sjbs.2018.11.005
Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci 10:103
Hayat R, Ali S, Amara U et al (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598
Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J Environ Qual 36:904–912. https://doi.org/10.2134/jeq2006.0425sc
Hu L, Robert CAM, Cadot S et al (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun. https://doi.org/10.1038/s41467-018-05122-7
Hu Y, Xie W, Chen B (2020) Arbuscular mycorrhiza improved drought tolerance of maize seedlings by altering photosystem II efficiency and the levels of key metabolites. Chem Biol Technol Agric. https://doi.org/10.1186/s40538-020-00186-4
Huang YM, Zou YN, Wu QS (2017) Alleviation of drought stress by mycorrhizas is related to increased root H2O2 efflux in trifoliate orange. Sci Rep 7:1–9. https://doi.org/10.1038/srep42335
Huanglongbing C, Gottwald TR (2010) Current epidemiological understanding of. Annu Rev Phytopathol. https://doi.org/10.1146/annurev-phyto-073009
Hussain HA, Hussain S, Khaliq A et al (2018) Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Front Plant Sci 9:393
Hwang E-Y, Song Q, Jia G et al (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15:1–12
Ingrisch J, Karlowsky S, Anadon-Rosell A et al (2018) Land use alters the drought responses of productivity and CO2 fluxes in mountain grassland. Ecosystems 21:689–703. https://doi.org/10.1007/s10021-017-0178-0
Jacoby R, Peukert M, Succurro A et al (2017) The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01617
Jacoby RP, Chen L, Schwier M et al (2020) Recent advances in the role of plant metabolites in shaping the root microbiome. F100Res 9:151
Javid MG, Sorooshzadeh A, Moradi F et al (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5(6):726–734
Jia KP, Baz L, Al-Babili S (2018) From carotenoids to strigolactones. J Exp Bot 69:2189–2204
Johnová P, Skalák J, Saiz-Fernández I, Brzobohatý B (2016) Plant responses to ambient temperature fluctuations and water-limiting conditions: a proteome-wide perspective. Biochim Biophys Acta (BBA) Proteins Proteomics 1864:916–931. https://doi.org/10.1016/J.BBAPAP.2016.02.007
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33
Kalliola M, Jakobson L, Davidsson P et al (2020) Differential role of MAX2 and strigolactones in pathogen, ozone, and stomatal responses. Plant Direct 4:1–14. https://doi.org/10.1002/pld3.206
Kang SM, Radhakrishnan R, Khan AL et al (2014) Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84:115–124. https://doi.org/10.1016/j.plaphy.2014.09.001
Karlowsky S, Augusti A, Ingrisch J et al (2018a) Drought-induced accumulation of root exudates supports post-drought recovery of microbes in mountain grassland. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01593
Karlowsky S, Augusti A, Ingrisch J et al (2018b) Land use in mountain grasslands alters drought response and recovery of carbon allocation and plant-microbial interactions. J Ecol 106:1230–1243. https://doi.org/10.1111/1365-2745.12910
Karst J, Gaster J, Wiley E, Landhäusser SM (2017) Stress differentially causes roots of tree seedlings to exude carbon. Tree Physiol 37:154–164. https://doi.org/10.1093/treephys/tpw090
Kasim WA, Osman ME, Omar MN et al (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32:122–130. https://doi.org/10.1007/s00344-012-9283-7
Kaštovská E, Edwards K, Picek T, Šantrůčková H (2015) A larger investment into exudation by competitive versus conservative plants is connected to more coupled plant–microbe N cycling. Biogeochemistry 122:47–59
Kebede A, Kang MS, Bekele E (2019) Advances in mechanisms of drought tolerance in crops, with emphasis on barley. Adv Agron 156:265–314. https://doi.org/10.1016/bs.agron.2019.01.008
Khadka K, Earl HJ, Raizada MN, Navabi A (2020) A physio-morphological trait-based approach for breeding drought tolerant wheat. Front Plant Sci 11:715
Kim JI, Baek D, Park HC et al (2013) Overexpression of arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhance. Mol Plant 6:337–349. https://doi.org/10.1093/mp/sss100
Kohlen W, Charnikhova T, Liu Q et al (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host arabidopsis. Plant Physiol 155:974–987. https://doi.org/10.1104/pp.110.164640
Kollers S, Rodemann B, Ling J et al (2013) Whole genome association mapping of fusarium head blight resistance in European Winter wheat (Triticum aestivum L.). PLoS ONE. https://doi.org/10.1371/journal.pone.0057500
Kour D, Khan SS, Kaur T et al (2022) Drought adaptive microbes as bioinoculants for the horticultural crops. Heliyon 8:e09493
Kuila D, Ghosh S (2022) Aspects, problems and utilization of Arbuscular Mycorrhizal (AM) application as bio-fertilizer in sustainable agriculture. Curr Res Microb Sci 3:100107
Kumar M, Mishra S, Dixit V et al (2016) Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signal Behav 11:1–9. https://doi.org/10.1080/15592324.2015.1071004
Kurm V, van der Putten WH, de Boer W et al (2017) Low abundant soil bacteria can be metabolically versatile and fast growing. Ecology 98:555–564. https://doi.org/10.1002/ecy.1670
Lepsch HC, Brown PH, Peterson CA et al (2019) Impact of organic matter amendments on soil and tree water status in a California orchard. Agric Water Manag 222:204–212. https://doi.org/10.1016/j.agwat.2019.06.002
Li Y, Zhang J, Zhang J et al (2013) Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions. Plant Biotechnol J 11:747–758. https://doi.org/10.1111/pbi.12066
Liao D, Wang S, Cui M et al (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. Int J Mol Sci 19:3146
Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J (faisalabad) 29:201–208. https://doi.org/10.5423/PPJ.SI.02.2013.0021
Liu J, He H, Vitali M et al (2015) Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241:1435–1451. https://doi.org/10.1007/s00425-015-2266-8
Liu J, Lovisolo C, Schubert A, Cardinale F (2013) Signaling role of Strigolactones at the interface between plants, (micro)organisms, and a changing environment. J Plant Interact 8:17–33. https://doi.org/10.1080/17429145.2012.750692
Lo SF, Ho THD, Liu YL et al (2017) Ectopic expression of specific GA2 oxidase mutants promotes yield and stress tolerance in rice. Plant Biotechnol J 15:850–864. https://doi.org/10.1111/pbi.12681
López-Ráez JA, Kohlen W, Charnikhova T et al (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187:343–354. https://doi.org/10.1111/j.1469-8137.2010.03291.x
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/s0021-9258(19)52451-6
Lundberg DS, Lebeis SL, Herrera S et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Ma W, Tang S, Dengzeng Z et al (2022) Root exudates contribute to belowground ecosystem hotspots: a review. Front Microbiol 13:937940
Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Inoculation of Brassica oxyrrhina with plant growth promoting bacteria for the improvement of heavy metal phytoremediation under drought conditions. J Hazard Mater 320:36–44. https://doi.org/10.1016/j.jhazmat.2016.08.009
Martiny JBH, Martiny AC, Weihe C et al (2017) Microbial legacies alter decomposition in response to simulated global change. ISME J 11:490–499. https://doi.org/10.1038/ismej.2016.122
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Miller SB, Heuberger AL, Broeckling CD, Jahn CE (2019) Non-targeted metabolomics reveals sorghum rhizosphere-associated exudates are influenced by the belowground interaction of substrate and sorghum genotype. Int J Mol Sci. https://doi.org/10.3390/ijms20020431
Min Z, Li R, Chen L et al (2019) Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol Biochem 135:99–110. https://doi.org/10.1016/j.plaphy.2018.11.037
Moradtalab N, Hajiboland R, Aliasgharzad N et al (2019) Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 9:1–22. https://doi.org/10.3390/agronomy9010041
Mostofa MG, Li W, Nguyen KH et al (2018) Strigolactones in plant adaptation to abiotic stresses: an emerging avenue of plant research. Plant Cell Environ 41:2227–2243. https://doi.org/10.1111/pce.13364
Müller A, Eltigani A, George E (2019) The abundance of arbuscular mycorrhizal fungal species in symbiosis with okra plants is affected by induced drought conditions in a calcareous substrate. Rhizosphere 10:100150. https://doi.org/10.1016/J.RHISPH.2019.100150
Nasir F, Tian L, Shi S et al (2019) Strigolactones positively regulate defense against Magnaporthe oryzae in rice (Oryza sativa). Plant Physiol Biochem 142:106–116. https://doi.org/10.1016/j.plaphy.2019.06.028
Naveed M, Mitter B, Reichenauer TG et al (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39. https://doi.org/10.1016/j.envexpbot.2013.09.014
Nawaz F, Naeem M, Zulfiqar B et al (2017) Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: a critical review. Environ Sci Pollut Res 24:15959–15975. https://doi.org/10.1007/s11356-017-9163-6
Oburger E, Jones DL (2018) Sampling root exudates—mission impossible? Rhizosphere 6:116–133. https://doi.org/10.1016/j.rhisph.2018.06.004
Oppenheimer-Shaanan Y, Jakoby G, Starr ML et al (2022) A dynamic rhizosphere interplay between tree roots and soil bacteria under drought stress. Elife. https://doi.org/10.7554/ELIFE.79679
Ortiz N, Armada E, Duque E et al (2015) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96. https://doi.org/10.1016/J.JPLPH.2014.08.019
Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:86
Ouédraogo DY, Mortier F, Gourlet-Fleury S et al (2013) Slow-growing species cope best with drought: evidence from long-term measurements in a tropical semi-deciduous moist forest of Central Africa. J Ecol 101:1459–1470. https://doi.org/10.1111/1365-2745.12165
Pascale A, Proietti S, Pantelides IS, Stringlis IA (2020) Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front Plant Sci 10:1741
Pavithra D, Yapa N (2018) Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundw Sustain Dev 7:490–494. https://doi.org/10.1016/j.gsd.2018.03.005
Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiology 29(12):1513–1523. https://doi.org/10.1093/treephys/tpp083
Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999. https://doi.org/10.1111/j.1365-2435.2008.01495.x
Pospíšilová H, Jiskrová E, Vojta P et al (2016) Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnol 33:692–705. https://doi.org/10.1016/j.nbt.2015.12.005
Preece C, Farré-Armengol G, Llusià J, Peñuelas J (2018) Thirsty tree roots exude more carbon. Tree Physiol 38:690–695. https://doi.org/10.1093/treephys/tpx163
Preece C, Peñuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–17
Puig-Sirera À, Provenzano G, González-Altozano P et al (2021) Irrigation water saving strategies in Citrus orchards: analysis of the combined effects of timing and severity of soil water deficit. Agric Water Manag. https://doi.org/10.1016/j.agwat.2021.106773
Quiroga G, Erice G, Aroca R et al (2017) Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci 8:1–15. https://doi.org/10.3389/fpls.2017.01056
Rameau C, Bertheloot J, Leduc N et al (2015) Multiple pathways regulate shoot branching. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00741
Ray S, Mishra S, Bisen K et al (2018) Modulation in phenolic root exudate profile of Abelmoschus esculentus expressing activation of defense pathway. Microbiol Res 207:100–107. https://doi.org/10.1016/j.micres.2017.11.011
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
Ren CG, Kong CC, Xie ZH (2018) Role of abscisic acid in strigolactone-induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol. https://doi.org/10.1186/s12870-018-1292-7
Romano I, Ventorino V, Pepe O (2020) Effectiveness of plant beneficial microbes: overview of the methodological approaches for the assessment of root colonization and persistence. Front Plant Sci 11:6
Rovira AD HJR (1961) Plant root excretions rhizosphere, pp 199–214
Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556. https://doi.org/10.1104/pp.108.127613
Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J. Plant Physiol 167(11):862–869. https://doi.org/10.1016/j.jplph.2010.01.018
Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83. https://doi.org/10.1016/J.TPLANTS.2012.10.003
Ryan PR, Delhaize E, Watt M, Richardson AE (2016) Plant roots: understanding structure and function in an ocean of complexity. Ann Bot 118:555–559. https://doi.org/10.1093/aob/mcw192
Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Sedaghat M, Tahmasebi-Sarvestani Z, Emam Y, Mokhtassi-Bidgoli A (2017) Physiological and antioxidant responses of winter wheat cultivars to strigolactone and salicylic acid in drought. Plant Physiol Biochem 119:59–69. https://doi.org/10.1016/j.plaphy.2017.08.015
Seleiman MF, Al-Suhaibani N, Ali N et al (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants. https://doi.org/10.3390/plants
Seto Y, Sado A, Asami K et al (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci U S A 111:1640–1645. https://doi.org/10.1073/pnas.1314805111
Shanmugavadivel PS, Prakash C, Amitha Mithra S (2018) Molecular approaches for dissecting and improving drought and heat tolerance in rice. In: Advances in rice research for abiotic stress tolerance, pp 839–867. https://doi.org/10.1016/B978-0-12-814332-2.00042-3
Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54:78–88. https://doi.org/10.1016/j.plaphy.2012.02.001
Simon L, Haichar FZ (2019) Determination of root exudate concentration in the rhizosphere using 13C labeling. Bio Protoc 9:1–7. https://doi.org/10.21769/bioprotoc.3228
Sirko A, Wawrzyńska A, Brzywczy J, Sieńko M (2021) Control of ABA signaling and crosstalk with other hormones by the selective degradation of pathway components. Int J Mol Sci 22:4638
Sobhanian H, Pahlavan S, Meyfour A (2020) How does proteomics target plant environmental stresses in a semi-arid area? Mol Biol Rep 47:3181–3194
Song F, Han X, Zhu X, Herbert SJ (2012) Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages. Can J Soil Sci 92:501–507. https://doi.org/10.4141/CJSS2010-057
Staudinger C, Mehmeti-Tershani V, Gil-Quintana E et al (2016) Evidence for a rhizobia-induced drought stress response strategy in Medicago truncatula. J Proteomics 136:202–213. https://doi.org/10.1016/j.jprot.2016.01.006
Stes E, Depuydt S, de Keyser A et al (2015) Strigolactones as an auxiliary hormonal defence mechanism against leafy gall syndrome in Arabidopsis thaliana. J Exp Bot 66:5123–5134. https://doi.org/10.1093/jxb/erv309
Stringlis IA, Yu K, Feussner K et al (2018) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci U S A 115:E5213–E5222. https://doi.org/10.1073/pnas.1722335115
Su Q, Rowley KG, Balazs NDH (2002) Carotenoids: separation methods applicable to biological samples. J Chromatogr B 781:393–418
Sun X, Shi J, Ding G (2017) Combined effects of arbuscular mycorrhiza and drought stress on plant growth and mortality of forage sorghum. Appl Soil Ecol 119:384–391. https://doi.org/10.1016/j.apsoil.2017.07.030
Swain R, Sahoo S, Behera M, Rout GR (2023) Instigating prevalent abiotic stress resilience in crop by exogenous application of phytohormones and nutrient. Front Plant Sci 14:1104874
Tabassum T, Farooq M, Ahmad R et al (2018) Terminal drought and seed priming improves drought tolerance in wheat. Physiol Mol Biol Plants 24:845–856. https://doi.org/10.1007/s12298-018-0547-y
Teshome DT, Zharare GE, Naidoo S (2020) The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Front Plant Sci 11:1874
Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j.plaphy.2015.11.001
Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15:211–216. https://doi.org/10.1111/mpp.12074
Tzortzakis N, Chrysargyris A, Aziz A (2020) Adaptive response of a native Mediterranean grapevine cultivar upon short-term exposure to drought and heat stress in the context of climate change. Agronomy. https://doi.org/10.3390/agronomy10020249
Uma T, Ashwin R, Kale RD, Bagyaraj DJ (2017) Symbiotic response of Abelmoschus esculentus (Okra) to different arbuscular mycorrhizal fungi. J Soil Biol Ecol 37(1):19–25
van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265. https://doi.org/10.1016/j.tplants.2016.01.008
van Ha C, Leyva-Gonzalez MA, Osakabe Y et al (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci U S A 111:851–856. https://doi.org/10.1073/pnas.1322135111
Varshney RK, Terauchi R, Mccouch SR (2014) Harvesting the promising fruits of genomics: applying genome sequencing technologies to crop breeding. PLoS Biol. https://doi.org/10.1371/journal.pbio
Vélez-Sánchez JE, Balaguera-López HE, Alvarez-Herrera JG (2021) Effect of regulated deficit irrigation (RDI) on the production and quality of pear Triunfo de Viena variety under tropical conditions. Sci Hortic. https://doi.org/10.1016/j.scienta.2020.109880
Visentin I, Vitali M, Ferrero M et al (2016) Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol 212:954–963. https://doi.org/10.1111/nph.14190
Vranova V, Rejsek K, Skene KR et al (2013) Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. J Plant Nutr Soil Sci 176:175–199. https://doi.org/10.1002/jpln.201000360
Walker JM. Methods in molecular biology
Wang JY, Jamil M, Lin PY et al (2020) Efficient mimics for elucidating zaxinone biology and promoting agricultural applications. Mol Plant 13:1654–1661. https://doi.org/10.1016/j.molp.2020.08.009
Wang Q, Ni J, Shah F et al (2019) Overexpression of the stress-inducible SsMAX2 promotes drought and salt resistance via the regulation of redox homeostasis in arabidopsis. Int J Mol Sci 20:1–19. https://doi.org/10.3390/ijms20040837
Wang X, Kang W, Wu F et al (2022) Comparative transcriptome analysis reveals new insight of Alfalfa (Medicago sativa L.) cultivars in response to abrupt freezing stress. Front Plant Sci 13:1–15. https://doi.org/10.3389/fpls.2022.798118
Wani KI, Naeem M, Khan MMA, Aftab T (2023) Insights into strigolactone (GR24) mediated regulation of cadmium-induced changes and ROS metabolism in Artemisia annua. J Hazard Mater 448:130899. https://doi.org/10.1016/J.JHAZMAT.2023.130899
Wani KI, Zehra A, Choudhary S et al (2021) Mechanistic insights into strigolactone biosynthesis, signaling, and regulation during plant growth and development. J Plant Growth Regul 40:1836–1852
Wasaya A, Zhang X, Fang Q, Yan Z (2018) Root phenotyping for drought tolerance: a review. Agronomy. https://doi.org/10.3390/agronomy8110241
Waters MT, Brewer PB, Bussell JD et al (2012) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159:1073–1085. https://doi.org/10.1104/pp.112.196253
Williams A, de Vries FT (2020) Plant root exudation under drought: implications for ecosystem functioning. New Phytol 225:1899–1905. https://doi.org/10.1111/nph.16223
Xie X (2016) Structural diversity of strigolactones and their distribution in the plant kingdom. J Pestic Sci 41:175–180. https://doi.org/10.1584/jpestics.J16-02
Xu X, Fang P, Zhang H et al (2019) Strigolactones positively regulate defense against root-knot nematodes in tomato. J Exp Bot 70:1325–1337. https://doi.org/10.1093/jxb/ery439
Yang X, Jia Z, Pu Q et al (2022) ABA mediates plant development and abiotic stress via alternative splicing. Int J Mol Sci 23:3796
Yoneyama K, Brewer PB (2021) Strigolactones, how are they synthesized to regulate plant growth and development? Curr Opin Plant Biol 63:102072
Yoneyama K, Xie X, Yoneyama K et al (2018) Which are the major players, canonical or non-canonical strigolactones? J Exp Bot 69:2231–2239
Yooyongwech S, Samphumphuang T, Tisarum R et al (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117. https://doi.org/10.1016/j.scienta.2015.11.002
Zhalnina K, Louie KB, Hao Z et al (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480. https://doi.org/10.1038/s41564-018-0129-3
Zhang A, Sun H, Wang P et al (2012) Modern analytical techniques in metabolomics analysis. Analyst 137:293–300. https://doi.org/10.1039/c1an15605e
Zhang C, Feng C, Zheng Y et al (2020) Root exudates metabolic profiling suggests distinct defense mechanisms between resistant and susceptible tobacco cultivars against black shank disease. Front Plant Sci 11:1–15. https://doi.org/10.3389/fpls.2020.559775
Zhao L, Peng T, Chen CY et al (2019) HY5 interacts with the histone deacetylase HDA15 to repress hypocotyl cell elongation in photomorphogenesis. Plant Physiol 180:1450–1466. https://doi.org/10.1104/pp.19.00055
Zhu S, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333. https://doi.org/10.1016/j.apsoil.2016.07.009
Zhuang L, Wang J, Huang B (2017) Drought inhibition of tillering in Festuca arundinacea associated with axillary bud development and strigolactone signaling. Environ Exp Bot 142:15–23. https://doi.org/10.1016/j.envexpbot.2017.07.017
Zhang Y, van Dijk ADJ, Scaffidi A, Flematti GR, Hofmann M, Hofmann, Charnikhova T, Verstappen F, Hepworth J, Krol Svd, Leyser O, Smith S, Zwanenburg B, Al-Babili S, Ruyter-Spira C, Bouwmeester HJ (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol 10(12):1028–1033. https://doi.org/10.1038/nchembio.1660
Acknowledgements
We acknowledge the Department of Biotechnology (DBT), and Council for Scientific and Industrial Research (CSIR) for research funding in our lab. We also acknowledge National Institute of Plant Genome Research, New Delhi, India. In addition, NS acknowledges CSIR for providing senior research associate fellowship (Award No. 13(9170-A)/2021-Pool).
Funding
Funding was provided by Council of scientific and industrial Research, India (Award No. 13(9170-A)/2021-Pool).
Author information
Authors and Affiliations
Contributions
NS conceptualized and wrote the manuscript. NS, DC, and SKG edited and finalized the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest declared in the manuscript.
Additional information
Handling Editor: Tariq Aftab.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Singh, N., Chattopadhyay, D. & Gupta, S.K. Updating the Impact of Drought on Root Exudation: A Strigolactones Perspective. J Plant Growth Regul 42, 5131–5151 (2023). https://doi.org/10.1007/s00344-023-11061-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11061-5