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Root Exudates and Their Significance in Abiotic Stress Amelioration in Plants: A Review

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Abstract

Abiotic stresses such as salinity, drought, extreme temperature, radiation, nutrient deficiency, and heavy metals can significantly impact plant growth and yield, posing a challenge to agriculture. Various strategies have been employed to enhance plant resistance to these stresses through conventional and genetic manipulations. However, these often require extensive breeding programmes and substantial financial investments. In this regard, plant root exudates have emerged as a promising tool for improving plant performance under adverse conditions. They play a crucial role in the rhizosphere, influencing and guiding the microbial community to support plant growth. Published literature suggests that plants can adapt to abiotic stress by modifying the chemistry of their root exudates. These modified exudates can recruit beneficial microorganisms that aid in protecting plants from stress. Despite the progress made in identifying, characterizing, and detecting root exudates, there is still a substantial gap in our understanding of their significance and potential applications, particularly in addressing abiotic stress in plants. Therefore, the present review provides valuable insights into recent research progress in the field of root exudates. It covers fundamental information about root exudates, mechanisms of exudation, the impact of abiotic factors, and the interactions between roots and microbes in exudation. The review also explores how root exudates contribute to enhancing abiotic stress tolerance in plants, shedding light on the potential benefits of these compounds. The review also discusses existing challenges in the field of root exudates, particularly in their application for sustainable agriculture. It also addresses potential research gaps and outlines future directions for further investigation and practical application in agriculture for abiotic stress amelioration.

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References

  • Ahkami AH, WhiteHandakumbura RAPP, Jansson C (2017) Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3:233–243

    Article  Google Scholar 

  • Alengebawy A, Abdelkhalek ST, Qureshi SR, Wang MQ (2021) Heavy metals and pesticides toxicity in agricultural soil and plants: ecological risks and human health implications. Toxics 9(3):42. https://doi.org/10.3390/toxics9030042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali Q, Ashraf M (2011) Induction of drought tolerance in maize (Zea mays L.) due to exogenous application of trehalose: growth, photosynthesis, water relations and oxidative defence mechanism. J Agron Crop Sci 197:258–271

    Article  CAS  Google Scholar 

  • Ali SZ, Sandhya V, Grover M, Linga VR, Bandi V (2011) Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J Plant Interact 6:239–246

    Article  CAS  Google Scholar 

  • Ali Q, Anwar F, Ashraf M, Saari N, Perveen R (2013) Ameliorating effects of exogenously applied proline on seed composition, seed oil quality and oil antioxidant activity of maize (Zea mays L.) under drought stress. Int J Mol Sci 14:818–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angulo-Bejarano PI, Puente-Rivera J, Cruz-Ortega R (2021) Metal and metalloid toxicity in plants: an overview on molecular aspects. Plants (Basel) 10(4):635. https://doi.org/10.3390/plants10040635

    Article  CAS  PubMed  Google Scholar 

  • Anwer S, Ashraf MY, Hussain M, Ashraf M, Jamil A (2012) Citric acid mediated phytoextraction of cadmium by maize (Zea mays L.). Pak J Bot 44:1831–1836

    CAS  Google Scholar 

  • Badia MB, Maurino VG, Pavlovic T, Arias CL, Pagani MA, Andreo CS, Saigo M, Drincovich MF (2020) Loss of function of Arabidopsis NADP-malic enzyme 1 results in enhanced tolerance to aluminium stress. Plant J 101:653–665

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Peña C, Jasinski M, Santelia D, Martinoia E, Sumner LW (2008a) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146:762–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008b) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179:209–223

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Weir TL, Van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Broeckling CD, Vivanco JM (2010) Root secretion of phytochemicals in Arabidopsis is predominantly not influenced by diurnal rhythms. Mol Plant 3:491–498

    Article  CAS  PubMed  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19(2):90–98

    Article  CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The soil-borne legacy. Cell 172:1178–1180

    Article  CAS  PubMed  Google Scholar 

  • Banasiak J, Jasiński M (2022) ATP-binding cassette transporters in nonmodel plants. New Phytol 233(4):1597–1612

    Article  CAS  PubMed  Google Scholar 

  • Battey NH, Blackbourn HD (1993) The control of exocytosis in plant cells. New Phytol 125:307–308

    Article  CAS  PubMed  Google Scholar 

  • Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bekkara F, Jay M, Viricel MR, Rome S (1998) Distribution of phenolic compounds within seed and seedlings of two Vicia faba cvs differing in their see tannin content and study of their seed and root phenolic exudations. Plant Soil 203:27–36

    Article  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Bhardwaj AK, Arya G, Kumar R, Hamed L, Pirasteh-Anosheh H, Jasrotia P, Kashyap PL, Singh GP (2022) Switching to nanonutrients for sustaining agroecosystems and environment: the challenges and benefits in moving up from ionic to particle feeding. J Nanobiotechnol 20:19. https://doi.org/10.1186/s12951-021-01177-9

    Article  CAS  Google Scholar 

  • Bharti N, Pandey SS, Barnawal D, Kumar V, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhat MA, Kumar V, Bhat MA, Wani IA, Dar FL, Farooq I, Bhatti F, Koser R et al (2020) Mechanistic insights of the interaction of plant growth-promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front Microbiol 11:1952

    Article  PubMed  PubMed Central  Google Scholar 

  • Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley centre climate model. J Hydrometeorol 7:1113–1125

    Article  ADS  Google Scholar 

  • Calvo OC, Franzaring J, Schmid I, Müller M, Brohon N, Fangmeier A (2017) Atmospheric CO2 enrichment and drought stress modify root exudation of barley. Glob Change Biol 23:1292–1304

    Article  ADS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157. https://doi.org/10.3389/fpls.2019.00157

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wiren N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174:3–11. https://doi.org/10.1002/jpln.201000085

    Article  CAS  Google Scholar 

  • Chai YN, Schachtman DP (2022) Root exudates impact plant performance under abiotic stress. Trends Plant Sci 27:80–91

    Article  CAS  PubMed  Google Scholar 

  • Chandra D, Srivastava R, Glick BR, Sharma AK (2020) Rhizobacteria producing ACC deaminase mitigate water-stress response in finger millet (Eleusine coracana (L.) Gaertn.). Biotech 10:65

    Google Scholar 

  • Chen HJ, Hou WC, Kuc J, Lin YH (2001) Ca2+-dependent and Ca2+-independent excretion modes of salicylic acid in tobacco cell suspension culture. J Exp Bot 52:1219–1226

    CAS  PubMed  Google Scholar 

  • Chen Y, Yao Z, Sun Y, Wang E, Tian C, Sun Y, Liu J, Sun C (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daei G, Ardekani MR, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 66:617–625

    Article  Google Scholar 

  • Dardanelli MS, Manyani H, González-Barroso S, Rodríguez-Carvajal MA, Gil-Serrano AM, Espuny MR, López-Baena J, Bellogín RA (2010) Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483–493

    Article  CAS  Google Scholar 

  • Dardanelli MS, de Córdoba FJF, Estévez J, Contreras R, Cubo MT, Rodríguez-Carvajal MA, Gil-Serrano AM, López-Baena FJ (2012) Changes in flavonoids secreted by Phaseolus vulgaris roots in the presence of salt and the plant growth-promoting rhizobacterium Chryseobacterium balustinum. Appl Soil Ecol 57:31–38

    Article  Google Scholar 

  • De Andrade SAL, Borghi AA, De Oliveira VH, Gouveia LdM, Martins API, Mazzafera P (2022) Phosphorus shortage induces an increase in root exudation in fifteen Eucalypts species. Agronomy 12(9):2041. https://doi.org/10.3390/agronomy12092041

    Article  CAS  Google Scholar 

  • De Schepper V, De Swaef T, Bauweraerts I, Steppe K (2013) Phloem transport: a review of mechanisms and controls. J Exp Bot 64:4839–4850

    Article  PubMed  Google Scholar 

  • Deng L, Luo L, Li Y, Wang L, Zhang J, Zi B, Ye C, Liu Y, Huang H, Mei X, Deng W, He X, Zhu S, Min Yang M (2023) Autotoxic ginsenoside stress induces changes in root exudates to recruit the beneficial Burkholderia Strain B36 as revealed by transcriptomic and metabolomic approaches. J Agric Food Chem 71(11):4536–4549. https://doi.org/10.1021/acs.jafc.3c00311

    Article  CAS  PubMed  Google Scholar 

  • Dilnashin H, Birla H, Hoat TX, Singh HB, Singh SP, Keswani C (2020) Applications of agriculturally important microorganisms for sustainable crop production. Molecular aspects of plant beneficial microbes in agriculture. Academic Press, Cambridge, pp 403–415

    Chapter  Google Scholar 

  • Ding L, Li Y, Wang Y, Gao L, Wang M, Chaumont F, Shen Q, Guo S (2016) Root ABA accumulation enhances rice seedling drought tolerance under ammonium supply: interaction with aquaporins. Front Plant Sci 7:1206

    Article  PubMed  PubMed Central  Google Scholar 

  • Dinkeloo K, Boyd S, Pilot G (2018) Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Semin Cell Dev Biol 74:105–113

    Article  CAS  PubMed  Google Scholar 

  • Doneva D, Pal M, Brankova L, Szalai G, Tajti J, Khalil R, Ivanovska B, Velikova V (2021) The effects of putrescine pre-treatment on osmotic stress responses in drought-tolerant and drought-sensitive wheat seedlings. Physiol Plant 171:200–216

    Article  CAS  PubMed  Google Scholar 

  • Driouich A, Gaudry A, Pawlak B, Moore JP (2021) Root cap-derived cells and mucilage: a protective network at the root tip. Protoplasma 258(6):1179–1185. https://doi.org/10.1007/s00709-021-01660-y

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi P, Sopory SK (2023) Unravelling the mechanism of stress responses in crop plants. J Plant Growth Regul. https://doi.org/10.1007/s00344-023-11104-x

    Article  Google Scholar 

  • El-Daim IAA, Bejai S, Meijer J (2014) Improved heat stress tolerance of wheat seedlings by bacterial seed treatment. Plant Soil 379:337–350

    Article  Google Scholar 

  • ElGhazali GEB (2020) Suaeda vermiculata Forssk ex. J.F. Gmel.: structural characteristics and adaptations to salinity and drought: a review. Intermt J Sci 9:28–33. https://doi.org/10.18483/ijSci.2268

    Article  Google Scholar 

  • El-Hawary M, Nashed ME (2019) Effect of foliar application by some antioxidants on growth and productivity of maize under saline soil conditions. J Plant Prod 10:93–99

    Google Scholar 

  • Elkeilsh A, Awad YM, Soliman MH, Abu-Elsaoud A, Abdelhamid MT, El-Metwally IM (2019) Exogenous application of b-sitosterol mediated growth and yield improvement in water-stressed wheat (Triticum aestivum) involves up-regulated antioxidant system. J Plant Res 132:881–901

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant 31:937–945

    Article  CAS  Google Scholar 

  • Feng H, Fu R, Hou X, Lv Y, Zhang N, Liu Y, Xu Z, Miao Y (2021) Chemotaxis of beneficial rhizobacteria to root exudates: the first step towards root–microbe rhizosphere interactions. Int J Mol Sci 22(13):6655. https://doi.org/10.3390/ijms22136655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Field B, Jordan F, Osbourn A (2006) First encounters—deployment of defence-related natural products by plants. New Phytol 172:193–207

    Article  CAS  PubMed  Google Scholar 

  • Fujii K, Hayakawa C (2021) Root exudation and biodegradation of organic acids in a tropical forest soil under dipterocarp and pioneer trees. Plant Soil 469:213–226. https://doi.org/10.1007/s11104-021-05132-3

    Article  CAS  Google Scholar 

  • Gani U, Vishwakarma RA, Misra P (2021) Membrane transporters: the key drivers of transport of secondary metabolites in plants. Plant Cell Rep 40:1–18. https://doi.org/10.1007/s00299-020-02599-9

    Article  CAS  PubMed  Google Scholar 

  • Gargallo-Garriga A, Preece C, Sardans J, Oravec M, Urban O, Penuelas J (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep 8:1–15

    Article  CAS  Google Scholar 

  • Ghafoor R, Akram NA, Rashid M, Ashraf M, Iqbal M, Lixin Z (2019) Exogenously applied proline induced changes in key anatomical features and physio-biochemical attributes in water stressed oat (Avena sativa L.) plants. Physiol Mol Biol Plants 25:1121–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghuge SA, Nikalje GC, Kadam US, Suprasanna P, Hong JC (2023) Comprehensive mechanisms of heavy metal toxicity in plants, detoxification, and remediation. J Hazard Mater 450:131039

    Article  CAS  PubMed  Google Scholar 

  • Gill RA, Kanwar MK, Rodrigues dos Reis A, Ali B (2022) Editorial: heavy metal toxicity in plants: recent insights on physiological and molecular aspects. Front Plant Sci 12:830682. https://doi.org/10.3389/fpls.2021.830682

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomez-Zepeda D, Frausto M, Nájera-González HR, Herrera-Estrella L, Ordaz-Ortiz JJ (2021) Mass spectrometry-based quantification and spatial localization of small organic acid exudates in plant roots under phosphorus deficiency and aluminium toxicity. Plant J 106:1791–1806

    Article  CAS  PubMed  Google Scholar 

  • Grotewold E (2004) The challenges of moving chemicals within and out of cells: Insights into the transport of plant natural products. Planta 219:906–909

    Article  CAS  PubMed  Google Scholar 

  • Grover M, Madhubala R, Ali SZ, Yadav SK, Venkateswarlu B (2014) Influence of Bacillus spp. strains on seedling growth and physiological parameters of sorghum under moisture stress conditions. J Basic Microbiol 54:951–961

    Article  CAS  PubMed  Google Scholar 

  • Gulati S, Ballhausen MB, Kulkarni P, Grosch R, Garbeva P (2020) A non-invasive soil-based setup to study tomato root volatiles released by healthy and infected roots. Sci Rep 10(1):1–11. https://doi.org/10.1038/s41598-020-69468-z

    Article  CAS  Google Scholar 

  • Guo Z, Qin Y, Lv J, Wang X, Ye T, Dong X, Du N, Zhang T, Piao F, Dong H, Shen S (2023) High red/far-red ratio promotes root colonization of Serratia plymuthica A21–4 in tomato by root exudates-stimulated chemotaxis and biofilm formation. Plant Biochem. https://doi.org/10.1101/2023.07.06.547930

    Article  Google Scholar 

  • Han-Chen Z, Ferdinand SL, Xing-Kai Y, Yan Z, Shu W (2020) Analysis of terpene synthase family genes in Camellia sinensis with an emphasis on abiotic stress conditions. Sci Rep 10:933

    Article  ADS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Rahman A, Inafuku M, Oku H, Fujita M (2018) Exogenous nitric oxide donor and arginine provide protection against short-term drought stress in wheat seedlings. Physiol Mol Biol Plants 24:993–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassan N, Ebeed H, Aljaarany A (2020) Exogenous application of spermine and putrescine mitigate adversities of drought stress in wheat by protecting membranes and chloroplast ultra-structure. Physiol Mol Biol Plants 26:233–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatfield JL, Rueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extremes 10:4–10

    Article  Google Scholar 

  • Hayat S, Faraz A, Faizan M (2017) Root exudates: composition and impact on plant-microbe interaction. In: Ahmad I, Husain FM (eds) Biofilms in plant and soil health. John Wiley & Sons Ltd., Hoboken, pp 179–193

    Chapter  Google Scholar 

  • He YM, Zhan FD, Li Y, Xu WW, Zu YQ, Yue M (2016) Effect of enhanced UV-B radiation on methane emission in a paddy field and rice root exudation of low-molecular-weight organic acids. Photochem Photobiol Sci 15(6):735–737

    Article  CAS  PubMed  Google Scholar 

  • Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheat grass root exudation caused by food, drought, and nutrient stress. J Environ Qual 36:904–912

    Article  CAS  PubMed  Google Scholar 

  • Hiltner L (1904) Uber neure erfahrungen und probleme auf dem Gebiet der Boden-bakteriologie und unter besondere Berucksichtigung der grundungung und Bracke. Arbeit Deut Landw Ges Berlin 98:59–78

    Google Scholar 

  • Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminium tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu H, Tang C, Rengel Z (2005) Role of phenolics and organic acids in phosphorus mobilization in calcareous and acidic soils. J Plant Nutr 28:1427–1439

    Article  CAS  Google Scholar 

  • Huang H, Lu R, Zhan J, He J, Wang Y, Li T (2023) Role of root exudates in cadmium accumulation of a low-cadmium-accumulating tobacco line (Nicotiana tabacum L.). Toxics 11(2):141. https://doi.org/10.3390/toxics11020141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurley BA, Tran HT, Marty NJ, Park J, Snedden WA, Mullen RT, Plaxton WC (2010) The dual-targeted purple acid phosphatase isozyme AtPAP26 is essential for efficient acclimation of Arabidopsis to nutritional phosphate deprivation. Plant Physiol 153:1112–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilyas N, Mumtaz K, Akhtar N, Yasmin H, Sayyed RZ, Khan W, Enshasy HAE, Dailin DJ, Elsayed EA, Ali Z (2020) Exopolysaccharides producing bacteria for the amelioration of drought stress in wheat. Sustainability 12(21):8876. https://doi.org/10.3390/su12218876

    Article  CAS  Google Scholar 

  • Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaiswal SK, Naamala J, Dakora FD (2018) Nature and mechanisms of aluminium toxicity, tolerance and amelioration in symbiotic legumes and rhizobia. Biol Fertil Soils 54:309–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Javed MT, Saleem MH, Aslam S, Rehman M, Iqbal N, Begum R, Ali S, Alsahli AA (2020) Elucidating silicon-mediated distinct morpho-physio-biochemical attributes and organic acid exudation patterns of cadmium stressed Ajwain (Trachyspermum ammi L.). Plant Physiol Biochem 157:23–37

    Article  CAS  PubMed  Google Scholar 

  • Jogawat A, Yadav B, Chhaya NOP (2021) Metal transporters in organelles and their roles in heavy metal transportation and sequestration mechanisms in plants. Physiol Plant 173:259–275

    CAS  PubMed  Google Scholar 

  • Jousset A, Schulz W, Scheu S et al (2011) Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J 5:1108–1114. https://doi.org/10.1038/ismej.2011.9

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaci Y, Heyraud A, Barakat M, Heulin T (2005) Isolation and identification of an EPS producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res Microbiol 156:522–531

    Article  CAS  PubMed  Google Scholar 

  • Kandoudi W, Németh-Zámboriné É (2022) Stimulating secondary compound accumulation by elicitation: Is it a realistic tool in medicinal plants in vivo? Phytochem Rev 21:2007–2025. https://doi.org/10.1007/s11101-022-09822-3

    Article  CAS  Google Scholar 

  • Kashyap PL, Rai P, Srivastava AK, Kumar S (2017) Trichoderma for climate resilient agriculture. World J Microbiol Biotechnol 33:155. https://doi.org/10.1007/s11274-017-2319-1

    Article  PubMed  Google Scholar 

  • Kashyap PL, Rai P, Kumar R, Sharma S, Jasrotia P, Srivastava AK et al (2018) Microbial nanotechnology for climate resilient agriculture. Microbes for climate resilient agriculture. Wiley, Hoboken, pp 279–344

    Chapter  Google Scholar 

  • Kashyap PL, Solanki MK, Kushwaha P, Srivastava KS (2020) Biocontrol potential of salt-tolerant Trichoderma and hypocrea isolates for the management of tomato root rot under saline environment. J Soil Sci Plant Nutr 20:160–176. https://doi.org/10.1007/s42729-019-00114-y

    Article  CAS  Google Scholar 

  • Kashyap PL, Kumar S, Aggarwal SK, Kaul N, Jasrotia P, Gupta A, Singh GP (2021) Resistance inducers and their role in reinforcing wheat defense system against fungal pathogens. J Cereal Res 13(3):229–254. https://doi.org/10.25174/2582-2675/2022/112810

    Article  Google Scholar 

  • Kashyap PL, Kumar S, Jasrotia P, Kumar RS, Sharma A, Tripathi R, Singh DP, Singh GP (2022) Induced resistance for sustainable management of wheat diseases. In: Sengar R, Chaudhary R, Bhadauriya H (eds) Handbook of research on green technologies for sustainable management of agricultural resources. IGI Global, Hershey, pp 385–408

    Chapter  Google Scholar 

  • Khan N, Ali S, Shahid MA, Mustafa A, Sayyed RZ, Curá JA (2021) Insights into the interactions among roots, rhizosphere, and rhizobacteria for improving plant growth and tolerance to abiotic stresses: a review. Cells 10:1551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidd P, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352

    CAS  PubMed  Google Scholar 

  • Knudson L (1920) The secretion of invertase by plant roots. Am J Bot 7:371–379

    Article  CAS  Google Scholar 

  • Kobayashi Y, Lakshmanan V, Kobayashi Y, Asai M, Iuchi S, Kobayashi M, Bais HP, Koyama H (2013) Overexpression of AtALMT1 in the Arabidopsis thaliana ecotype Columbia results in enhanced Al-activated malate excretion and beneficial bacterium recruitment. Plant Signal Behav 8:e25565

    Article  PubMed  PubMed Central  Google Scholar 

  • Koprivova A, Kopriva S (2022) Plant secondary metabolites altering root microbiome composition and function. Curr Opin Plant Biol 67:102227

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Urban MO, Prášil IT, Renaut J (2018) Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front Plant Sci 9:122

    Article  PubMed  PubMed Central  Google Scholar 

  • Kubi J (2005) The effect of exogenous spermidine on superoxide dismutase activity, H2O2 and superoxide radical level in barley leaves under water deficit conditions. Acta Physiol Plant 27:289–295

    Article  Google Scholar 

  • Kumar R, Kumar S, Srivastava S, Kashyap PL, Kumar A, Shekhar RK, Singh GP (2022) Rhizosphere microbes and wheat health management. In: Singh UB, Sahu PK, Singh HV, Sharma PK, Sharma SK (eds) Rhizosphere microbes: microorganisms for sustainability. Springer, Singapore, pp 223–242

    Chapter  Google Scholar 

  • Kumari S, Vaishnav A, Jain S, Varma A, Choudhary DK (2015) Bacterial-mediated induction of systemic tolerance to salinity with expression of stress alleviating enzymes in soybean (Glycine max L. Merrill). J Plant Growth Regul 34:558–573

    Article  CAS  Google Scholar 

  • Kumari B, Mallick MA, Solanki MK, Solanki AC, Hora A, Guo W (2019) Plant growth promoting rhizobacteria (PGPR): modern prospects for sustainable agriculture. In: Ansari R, Mahmood I (eds) Plant health under biotic stress. Springer, Singapore, pp 109–127

    Chapter  Google Scholar 

  • Kumawat C, Kumar A, Parshad J, Sharma SS, Patra A, Dogra P, Yadav GK, Dadhich SK, Verma R, Kumawat GL (2022) Microbial diversity and adaptation under salt-affected soils: a review. Sustainability 14:9280

    Article  CAS  Google Scholar 

  • Kushwaha P, Kashyap PL (2021) A review of advances in bioremediation of heavy metals by microbes and plants. J Nat Resour Conserv Manag 2(1):65–80

    Google Scholar 

  • Lee YH, Foster J, Chen J, Voll LM, Weber AP, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50:305–319

    Article  CAS  PubMed  Google Scholar 

  • Leng Z, Wu Y, Li J, Nie Z, Jia H, Yan C, Hong H, Wang X, Du D (2022) Phenolic root exudates enhance Avicennia marina tolerance to cadmium under the mediation of functional bacteria in mangrove sediments. Mar Pollut Bull 185(Pt A):114227. https://doi.org/10.1016/j.marpolbul.2022.114227

    Article  CAS  PubMed  Google Scholar 

  • Leuschner C, Tückmantel T, Meier IC (2022) Temperature effects on root exudation in mature beech (Fagus sylvatica L.) forests along an elevational gradient. Plant Soil 481:147–163. https://doi.org/10.1007/s11104-1800022-05629-5

    Article  CAS  Google Scholar 

  • Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot 94(2):297–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Lu H, Liu J, Hong H, Yan C (2015) The influence of flavonoid amendment on the absorption of cadmium in Avicennia marina roots. Ecotoxicol Environ Saf 120:1–6. https://doi.org/10.1016/j.ecoenv.2015.05.004

    Article  ADS  CAS  PubMed  Google Scholar 

  • Li GX, Wu XQ, Ye JR, Yang HC (2018a) Characteristics of organic acid secretion associated with the interaction between Burkholderia multivorans WS-FJ9 and poplar root system. Bio Med Res Int 2018:9619724

    Google Scholar 

  • Li L, Gu W, Li J, Li C, Xie T, Qu D, Meng Y, Li C (2018b) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiol Biochem 129:35–55

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Wu Y, Wang J, Yang B, Chen J, Wu H, Zhang Z, Lu C, Lin W, Wu L (2020) Linking short-chain N-acyl homoserine lactone-mediated quorum sensing and replant disease: a case study of rehmannia glutinosa. Front Plant Sci 11:787. https://doi.org/10.3389/fpls.2020.00787

    Article  PubMed  PubMed Central  Google Scholar 

  • Li G, Wang K, Qin Q, Li Q, Mo F, Nangia V, Liu Y (2023) Integrated microbiome and metabolomic analysis reveal responses of rhizosphere bacterial communities and root exudate composition to drought and genotype in rice (Oryza sativa L.). Rice 16:19. https://doi.org/10.1186/s12284-023-00636-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Magalhaes JV, Shaf J, Kochian LV (2009) Aluminium-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminium tolerance. Plant J 57:389–399

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Brettell LE, Qiu Z, Singh BK (2020) Microbiome-mediated stress resistance in plants. Trends Plant Sci 25:733–743

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Li J, Carvalhais LC, Percy CD, Prakash Verma J, Schenk PM et al (2021) Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogens. New Phytol 229(5):2873–2885. https://doi.org/10.1111/nph.17057

    Article  CAS  PubMed  Google Scholar 

  • Lombardi N, Vitale S, Turrà D, Reverberi M, Fanelli C, Vinale F, Marra R, Ruocco M, Pascale A, d’Errico G, Woo SL, Lorito M (2018) Root exudates of stressed plants stimulate and attract Trichoderma soil fungi. Mol Plant Microbe Interact 31(10):982–994. https://doi.org/10.1094/MPMI-12-17-0310-R

    Article  CAS  PubMed  Google Scholar 

  • Loyola-Vargas VM, Broeckling CD, Dayakar BV, Vivanco JM (2007) Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta 225:301–310

    Article  CAS  PubMed  Google Scholar 

  • Luo Q, Sun L, Hu X, Zhou R (2014) The variation of root exudates from the hyperaccumulator Sedum alfredii under cadmium stress: metabolomics analysis. PLoS ONE 9:e115581

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Luo Q, Wang S, Sun LN, Wang H (2017) Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Sci Rep 7:39878. https://doi.org/10.1038/srep39878

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon TL, Wilson JK (1921) Liberation of organic matter by roots of growing plants. Cornell University, New York

    Google Scholar 

  • Ma W, Tang S, Dengzeng Z, Zhang D, Zhang T, Ma X (2022a) Root exudates contribute to belowground ecosystem hotspots: a review. Front Microbiol 13:937940. https://doi.org/10.3389/fmicb.2022.937940

    Article  PubMed  PubMed Central  Google Scholar 

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses. Crop Sci 40:923–940

    Article  CAS  Google Scholar 

  • Manck-Götzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcinska I, Dziurka K, Waligorski P, Janowiak F, Skrzypek E, Warchoł M, Juzon K, Kapłoniak K (2020) Exogenous polyamines only indirectly induce stress tolerance in wheat growing in hydroponic culture under polyethylene glycol-induced osmotic stress. Life 10:151

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin BC, Gleeson D, Statton J, Siebers AR, Grierson P, Ryan MH et al (2018) Low light availability alters root exudation and reduces putative beneficial microorganisms in seagrass roots. Front Microbiol 8:02667

    Article  Google Scholar 

  • Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–543

    Article  CAS  PubMed  Google Scholar 

  • Meena M, Yadav G, Sonigra P, Nagda A, Mehta T, Swapnil P, Harish MA (2023) Role of elicitors to initiate the induction of systemic resistance in plants to biotic stress. Plant Stress 5:100103. https://doi.org/10.1016/j.stress.2022.100103

    Article  Google Scholar 

  • Mei PP, Gui LG, Wang P, Huang JC, Long HY, Christie P, Li L (2012) Maize/faba bean intercropping with rhizobia inoculation enhances productivity and recovery of fertilizer P in a reclaimed desert soil. Field Crops Res 130:19–27. https://doi.org/10.1016/j.fcr.2012.02.007

    Article  Google Scholar 

  • Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, Mukherjee PK (2018) Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fungal Biol Rev 32:62–85

    Article  Google Scholar 

  • Meyer S, De Angeli A, Fernie AR, Martinoia E (2010) Intra- and extra-cellular excretion of carboxylates. Trends Plant Sci 15:40–47

    Article  CAS  PubMed  Google Scholar 

  • Mishra AK, Sudalaimuthuasari N, Hazzouri KM, Saeed EE, Shah I, Amiri KMA (2022) Tapping into plant-microbiome interactions through the lens of multi-omics techniques. Cells 11(20):3254. https://doi.org/10.3390/cells11203254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moghaddam JA, Boehringer N, Burdziak A, Kunte HJ, Galinski EA, Schäberle TF (2016) Different strategies of osmoadaptation in the closely related marine myxobacteria Enhygromyxa salina SWB007 and Plesiocystis pacifica SIR-1. Microbiology 162:651–661

    Article  CAS  PubMed  Google Scholar 

  • Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J, Jiménez-Domínguez G, Chávez-Calvillo G (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci USA 25:E3563–E3572

    Google Scholar 

  • Morcillo RJ, Manzanera M (2021) The effects of plant-associated bacterial exopolysaccharides on plant abiotic stress tolerance. Metabolites 11:337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira H, Pereira SI, Vega A, Castro PM, Marques AP (2020) Synergistic effects of arbuscular mycorrhizal fungi and plant growth-promoting bacteria benefit maize growth under increasing soil salinity. J Environ Manag 257:109982

    Article  CAS  Google Scholar 

  • Münch E (1930) Die stoffbewegungen in der pflanze (Gustav Fischer, Jena). Curr Opin Plant Biol 43:36–42

    Google Scholar 

  • Mwendwa JM, Weston PA, Weidenhamer JD, Fomsgaard IS, Wu HW, Saliya G et al (2021) Metabolic profling of benzoxazinoids in the roots and rhizosphere of commercial winter wheat genotypes. Plant Soil 466:467–489. https://doi.org/10.1007/s11104-021-04996-9

    Article  CAS  Google Scholar 

  • Nair DS, Manjula S (2020) Induction of root endosymbiosis as a highly sustainable and efficient strategy for overproduction of the medicinally important diterpenoid lactone-andrographolide in Andrographis paniculata (Burm. F.) Wall. ex Nees. Ind Crops Prod 156:112835

    Article  CAS  Google Scholar 

  • Navada S, Vadstein O, Gaumet F, Tveten AK, Spanu C, Mikkelsen Ø, Kolarevic J (2020) Biofilms remember: osmotic stress priming as a microbial management strategy for improving salinity acclimation in nitrifying biofilms. Water Res 176:115732. https://doi.org/10.1016/j.watres.2020.115732

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

    Article  CAS  Google Scholar 

  • Ndour PMS, Heulin T, Achouak W, Laplaze L, Cournac L (2020) The rhizosheath: from desert plants adaptation to crop breeding. Plant Soil 456:1–13

    Article  CAS  Google Scholar 

  • Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS ONE 7:e35498

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11

    Article  PubMed  Google Scholar 

  • Neumann G, Romheld V (2007) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 41–93

    Google Scholar 

  • Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37:13–116

    Article  Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120

    Article  CAS  Google Scholar 

  • Oliveros-Bastidas AJ, Macías FA, Molinillo JMG (2012) Mechanical impedance effects on growth, phenolics and 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3-one (DIMBOA) in root exudates of Zea mays L. Int J Res Agric for 2:225–234

    Google Scholar 

  • Ortiz R, Braun HJ, Crossa J, Crouch JH, Davenport G, Dixon J (2008) Wheat genetic resources enhancement by the international maize and wheat improvement center (CIMMYT). Genetics Resour Crop Evol 55:1095–1140

    Article  Google Scholar 

  • Pan T, Liu M, Kreslavski VD, Zharmukhamedov SK, Nie C, Yu M, Kuznetsov VV, Allakhverdiev SI, Shabala S (2021) Non-stomatal limitation of photosynthesis by soil salinity. Crit Rev Environ Sci Technol 51(8):791–825. https://doi.org/10.1080/10643389.2020.1735231

    Article  CAS  Google Scholar 

  • Panchal P, Miller AJ, Giri J (2021) Organic acids: versatile stress-response roles in plants. J Exp Bot 72(11):4038–4052. https://doi.org/10.1093/jxb/erab019

    Article  CAS  PubMed  Google Scholar 

  • Panchal P, Preece C, Peñuelas J, Giri J (2022) Soil carbon sequestration by root exudates. Trends Plant Sci 27:749–757

    Article  CAS  PubMed  Google Scholar 

  • Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandiyan K, Kushwaha P, Srivastava R, Kashyap PL (2022) Metatranscriptomics of plant rhizosphere: a promising tool to decipher the role of microorganisms in plant growth and development. In: Singh UB, Rai JP, Sharma AK (eds) Re-visiting the rhizosphere eco-system for agricultural sustainability rhizosphere biology. Springer, Singapore, pp 491–509

    Chapter  Google Scholar 

  • Pang Z, Chen J, Wang T, Gao C, Li Z, Guo L, Xu J, Cheng Y (2021) Linking plant secondary metabolites and plant microbiomes: a review. Front Plant Sci 12:621276. https://doi.org/10.3389/fpls.2021.621276

    Article  PubMed  PubMed Central  Google Scholar 

  • Panthri M, Gupta M (2022) An insight into the act of iron to impede arsenic toxicity in paddy agro-system. J Environ Manag 316:115289. https://doi.org/10.1016/j.jenvman.2022.115289

    Article  CAS  Google Scholar 

  • Pantigoso HA, Manter DK, Fonte SJ, Vivanco JM (2023) Root exudate-derived compounds stimulate the phosphorus solubilizing ability of bacteria. Sci Rep 13:4050. https://doi.org/10.1038/s41598-023-30915-2

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathania P, Bhatia R, Khatri M (2020) Cross-competence and affectivity of maize rhizosphere bacteria Bacillus sp. MT7 in tomato rhizosphere. Sci Hortic 272:109480

    Article  CAS  Google Scholar 

  • Pérez-de-Luque A, Tille S, Johnson I, Pascual-Pardo D, Ton J, Cameron DD (2017) The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Sci Rep 7:1–10

    Article  Google Scholar 

  • Pramanik MHR, Nagai M, Asao T, Matsui Y (2000) Effects of temperature and photoperiod on phytotoxic root exudates of cucumber (Cucumis sativus) in hydroponic culture. J Chem Ecol 26:1953–1967

    Article  CAS  Google Scholar 

  • Rahimi S, Talebi M, Baninasab B, Gholami M, Zarei M, Shariatmadari H (2020) The role of plant growth-promoting rhizobacteria (PGPR) in improving iron acquisition by altering physiological and molecular responses in quince seedlings. Plant Physiol Biochem 155:406–415

    Article  CAS  PubMed  Google Scholar 

  • Rauf M, Awais M, Ud-Din A, Ali K, Gul H, Rahman MM, Hamayun M, Arif M (2021) Molecular mechanisms of the 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing Trichoderma asperellum map1 in enhancing wheat tolerance to waterlogging stress. Front Plant Sci 11:2213

    Article  Google Scholar 

  • Regaiolo A, Dominelli N, Andresen K, Heermann R (2020) The biocontrol agent and insect pathogen Photorhabdus luminescens interacts with plant roots. Appl Environ Microbiol 86:e00891-e920

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinnan R, Gehrke C, Michelsen A (2006) Two mire species respond differently to enhanced ultraviolet B radiation: effects on biomass allocation and root exudation. New Phytol 169(4):809

    Article  PubMed  Google Scholar 

  • Rolfe SA, Griffiths J, Ton J (2019) Crying out forhelp with root exudates: adaptive mechanisms by whichstressed plants assemble health-promoting soilmicrobiomes. Curr Opin Microbiol 49:73–82. https://doi.org/10.1016/j.mib.2019.10.003

    Article  CAS  PubMed  Google Scholar 

  • Ronco MG, Ruscitti MF, Arango MC, Beltrano J (2008) Glyphosate and mycorrhization induce changes in plant growth and in root morphology and architecture in pepper plants (Capsicum annuum L.). J Hortic Sci Biotechnol 83:497–505

    Article  CAS  Google Scholar 

  • Ross-Elliott TJ, Jensen KH, Haaning KS, Wager BM, Knoblauch J, Howell AH, Mullendore DL, Monteith AG (2017) Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. E Life 6:24125

    Google Scholar 

  • Rubio MB, Quijada NM, Perez E, Dominguez S, Monte E, Hermosa R (2014) Identifying beneficial qualities of Trichoderma parareesei for plants. Appl Environ Microbiol 80:1864–1873

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Ryan PR, James RA, Weligama C, Delhaize E, Rattey A, Lewis DC, Bovill WD, McDonald G (2014) Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat. Physiol Plant 151:230–242

    Article  CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Salem MA, Wang JY, Al-Babili S (2022) Metabolomics of plant root exudates: from sample preparation to data analysis. Front Plant Sci 13:1062982. https://doi.org/10.3389/fpls.2022.1062982

    Article  PubMed  PubMed Central  Google Scholar 

  • Samuel AL, Fernando M, Glass ADM (1992) Immunofluorescent localization of plasma membrane H+-ATPase in barley roots and effects of K nutrition. Plant Physiol 99:1509–1514

    Article  Google Scholar 

  • Sanchez-Fernandez R, Davies TGE, Coleman OD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244

    Article  CAS  PubMed  Google Scholar 

  • Sanders D, Bethke P (2000) Membrane transport. In: Buchanan BB, Gruisham W, Jones RL (eds) Biochemistry and molecular biology of plants. ASPP, Rockville, pp 110–158

    Google Scholar 

  • Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  CAS  PubMed  Google Scholar 

  • Sebastian A, Prasad M (2018) Exogenous citrate and malate alleviate cadmium stress in Oryza sativa L.: probing role of cadmium localization and iron nutrition. Ecotoxicol Environ Saf 166:215–222

    Article  CAS  PubMed  Google Scholar 

  • Semchenko M, Saar S, Lepik A (2014) Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. New Phytol 204:631–637

    Article  PubMed  Google Scholar 

  • Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ 25:333–341

    Article  PubMed  Google Scholar 

  • Sezgin A, Altuntasx C, Demiralay M, Cinemre S, Terzi R (2019) Exogenous alpha lipoic acid can stimulate photosystem II activity and the gene expressions of carbon fixation and chlorophyll metabolism enzymes in maize seedlings under drought. J Plant Physiol 232:65–73

    Article  CAS  PubMed  Google Scholar 

  • Sharipova G, Veselov D, Kudoyarova G, Fricke W, Dodd IC, Katsuhara M, Furuichi T, Ivanov I (2016) Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA-deficient barley mutant Az34. Ann Bot 118:777–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Kashyap PL, Srivastava AK, Bansal YK, Kaushik R (2019a) Isolation and characterization of halotolerant bacilli from chickpea (Cicer arietinum L.) rhizosphere for plant growth promotion and biocontrol traits. Eur J Plant Pathol 153:787–800. https://doi.org/10.1007/s10658-018-1592-7

    Article  CAS  Google Scholar 

  • Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Handa N, Kapoor D (2019b) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9:285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Saleh D, Charron J-B, Jabaji S (2020) A crosstalk between Brachypodium root exudates, organic acids, and Bacillus velezensis B26, a growth promoting bacterium. Front Microbiol 11:575578. https://doi.org/10.3389/fmicb.2020.575578

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharp R, Chen L, Davies WJ (2011) Inoculation of growing media with the rhizobacterium Variovorax paradoxus 5C–2 reduces unwanted stress responses in hardy ornamental species. Sci Hortic 129:804–811

    Article  Google Scholar 

  • Shaw AK, Bhardwaj PK, Ghosh S, Roy S, Saha S, Sherpa AR, Saha SK, Hossain Z (2016) β-Aminobutyric acid mediated drought stress alleviation in maize (Zea mays L.). Environ Sci Pollut Res 23:2437–2453

    Article  CAS  Google Scholar 

  • Shi L, Guo M, Ye N, Liu Y, Liu R, Xia Y, Cui S, Zhang J (2015) Reduced ABA accumulation in the root system is caused by ABA exudation in upland rice (Oryza sativa L. var. Gaoshan1) and this enhanced drought adaptation. Plant Cell Physiol 56:951–964

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Jha PN (2016) Mitigation of salt stress in wheat plant (Triticum aestivum) by ACC deaminase bacterium Enterobacter sp. SBP-6 isolated from Sorghum bicolor. Acta Physiol Plant 38:110

    Article  Google Scholar 

  • Singh R, Singh P, Sharma R (2014) Microorganism as a tool of bioremediation technology for cleaning environment: a review. Proc Int Acad Ecol Environ Sci 4:1–6

    ADS  CAS  Google Scholar 

  • Singh N, Chattopadhyay D, Gupta SK (2023) Updating the impact of drought on root exudation: a strigolactones perspective. J Plant Growth Regul 42:5131–5151. https://doi.org/10.1007/s00344-023-11061-5

    Article  CAS  Google Scholar 

  • Sisó-Terraza P, Rios JJ, Abadia J, Abadia A, Álvarez-Fernández A (2016) Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms. New Phytol 209(2):733–745

    Article  PubMed  Google Scholar 

  • Solanki MK, Kumar S, Pandey AK, Srivastava S, Singh RK, Kashyap PL, Srivastava AK, Arora DK (2012) Diversity and antagonistic potential of Bacillus spp. associated to the rhizosphere of tomato for the management of Rhizoctonia solani. Biocontrol Sci Technol 22(2):203–217

    Article  Google Scholar 

  • Solanki MK, Solanki AC, Rai S, Srivastava S, Kashyap BK, Divvela PK, Kumar S, Yandigeri MS, Kashyap PL, Shrivastava AK, Ali B, Khan S, Jaremko M, Qureshi KA (2022) Functional interplay between antagonistic bacteria and Rhizoctonia solani in the tomato plant rhizosphere. Front Microbiol 13:990850. https://doi.org/10.3389/fmicb.2022.990850

    Article  PubMed  PubMed Central  Google Scholar 

  • Somssich M, Khan GA, Persson S (2016) Cell wall heterogeneity in root development of Arabidopsis. Front Plant Sci 7:1242

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stohr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293–2303

    Article  CAS  PubMed  Google Scholar 

  • Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S, Van Verk MC, Berendsen RL, Bakker PAHM (2018a) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci USA 115:E5213–E5222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S, Van Verk MC, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018b) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci USA 115(22):E5213–E5222. https://doi.org/10.1073/pnas.1722335115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su F, Jacquard C, Villaume S, Michel J, Rabenoelina F, Clement C, Barka AB, Dhondt-Cordelier S (2015) Burkholderia phytofrmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci 6:810

    Article  PubMed  PubMed Central  Google Scholar 

  • Subiramani S, Ramalingam S, Muthu T, Nile SH, Venkidasamy B (2020) Development of abiotic stress tolerance in crops by plant growth-promoting rhizobacteria (PGPR). Phyto-microbiome in stress regulation. Environmental and microbial biotechnology. Springer, Singapore, pp 125–145

    Chapter  Google Scholar 

  • Sugiyama A (2019) The soybean rhizosphere: metabolites, microbes, and beyond—a review. J Adv Res 19:67–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavanoid in legume–Rhizobium symbiosis. Plant Physiol 144:2000–2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Q, Wang X, Ding S, Yuan X (2005) Effects of exogenous organic chelators on phytochelatins production and its relationship with cadmium toxicity in wheat (Triticum aestivum L.) under cadmium stress. Chemosphere 60:22–31

    Article  ADS  CAS  PubMed  Google Scholar 

  • Sun L, Cao X, Tan C, Deng Y, Cai R, Peng X, Bai J (2020) Analysis of the effect of cadmium stress on root exudates of Sedum plumbizincicola based on metabolomics. Ecotoxicol Environ Saf 205:111152. https://doi.org/10.1016/j.ecoenv.2020.111152

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Jiang S, Jiang C, Wu C, Gao M, Wang Q (2021a) A review of root exudates and rhizosphere microbiome for crop production. Environ Sci Pollut Res 28:54497–54510. https://doi.org/10.1007/s11356-021-15838-7

    Article  CAS  Google Scholar 

  • Sun Y, Tian L, Chang J, Shi S, Zhang J, Xie H, Cai Y, Chen D (2021b) Rice domestication influences the composition and function of the rhizosphere bacterial chemotaxis systems. Plant Soil 466:81–99

    Article  CAS  Google Scholar 

  • Tedone F, Dottore ED, Palladino M, Mazzolai B, Marcati P (2020) Optimal control of plant root tip dynamics in soil. Bioinspir Biomim 15:056006. https://doi.org/10.1088/1748-3190/ab9a15

    Article  PubMed  Google Scholar 

  • Timmusk S, El-Daim IAA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 9:e96086

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Tiziani R, Miras-Moreno B, Malacrinò A, Vescio R, Lucini L, Mimmo T, Cesco S, Sorgonà A (2022) Drought, heat, and their combination impact the root exudation patterns and rhizosphere microbiome in maize roots. Environ Exp Bot 203:105071. https://doi.org/10.1016/j.envexpbot.2022.105071

    Article  CAS  Google Scholar 

  • Tucci M, Ruocco M, De Masi L, De Palma M, Lorito M (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12:341–354

    Article  CAS  PubMed  Google Scholar 

  • Ulrich DEM, Sevanto S, Ryan M, Albright MBN, Johansen RB, Dunbar JM (2019) Plant-microbe interactions before drought influence plant physiological responses to subsequent severe drought. Sci Rep 9:249

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Ulrich DEM, Clendinen CS, Alongi F, Mueller RC, Chu RK, Toyoda J, Gallegos-Graves V, Goemann HM, Peyton B, Sevanto S, Dunbar J (2022) Root exudate composition reflects drought severity gradient in blue grama (Bouteloua gracilis). Sci Rep 12:12581. https://doi.org/10.1038/s41598-022-16408-8

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyay SK, Srivastava AK, Rajput VD, Chauhan PK, Bhojiya AA, Jain D, Chaubey G, Dwivedi P, Sharma B, Minkina T (2022) Root exudates: mechanistic insight of plant growth promoting rhizobacteria for sustainable crop production. Front Microbiol 13:916488. https://doi.org/10.3389/fmicb.2022.916488

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Heijden MGA, Bardgett RD, vanStraalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Verma SK, Sahu PK, Kumar K, Pal G, Gond SK, Kharwar RN, White JF (2021) Endophyte roles in nutrient acquisition, root system architecture development and oxidative stress tolerance. J Appl Microbiol 131(5):2161–2177

    Article  CAS  PubMed  Google Scholar 

  • Veroneze-Junior V, Martins M, Mc Leod L, Souza K, Santos-Filho PR, Magalhaes PC, Carvalho DT, Santos MH (2020) Leaf application of chitosan and physiological evaluation of maize hybrids contrasting for drought tolerance under water restriction. Braz J Biol 80:631–640

    Article  CAS  PubMed  Google Scholar 

  • Vidal A, Hirte J, Bender SF, Mayer J, Gattinger A, Höschen C, Schädler S, Iqbal TM (2018) Linking 3D soil structure and plant-microbe-soil carbon transfer in the rhizosphere. Front Environ Sci 6:9

    Article  Google Scholar 

  • Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2017) Citrus plants exude proline and phytohormones under abiotic stress conditions. Plant Cell Rep 36:1971–1984

    Article  CAS  PubMed  Google Scholar 

  • Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2018a) Salt stress alleviation in citrus plants by plant growth-promoting rhizobacteria Pseudomonas putida and Novosphingobium sp. Plant Cell Rep 37:1557–1569

    Article  CAS  PubMed  Google Scholar 

  • Vives-Peris V, Molina L, Segura A, Gomez-Cadenas A, Pérez-Clemente RM (2018b) Root exudates from citrus plants subjected to abiotic stress conditions have a positive effect on rhizobacteria. J Plant Physiol 228:208–217

    Article  CAS  PubMed  Google Scholar 

  • Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente RM (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39:3–17

    Article  CAS  PubMed  Google Scholar 

  • Walne CH, Reddy KR (2022) Temperature effects on the shoot and root growth, development, and biomass accumulation of corn (Zea mays L.). Agriculture 12(4):443. https://doi.org/10.3390/agriculture12040443

    Article  Google Scholar 

  • Wang Q, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct Plant Biol 43:161–172

    Article  PubMed  Google Scholar 

  • Wang G, Xiao Y, Deng X, Zhang H, Li T, Chen H (2018) Exogenous hydrogen peroxide contributes to heme oxygenase-1 delaying programmed cell death in isolated aleurone layers of rice subjected to drought stress in a cGMP-dependent manner. Front Plant Sci 9:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang D, Gao Y, Li M, Sturrock CJ, Gregory AS, Zhang X (2020) Change in hydraulic properties of the rhizosphere of maize under different abiotic stresses. Plant Soil 452:615–626

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304(5677):1629–1633

    Article  ADS  CAS  PubMed  Google Scholar 

  • Woo OG, Kim H, Kim JS, Keum HL, Lee KC, Sul WJ, Lee JH (2020) Bacillus subtilis strain GOT9 confers enhanced tolerance to drought and salt stresses in Arabidopsis thaliana and Brassica campestris. Plant Physiol Biochem 148:359–367

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Zhao C, Zhao X, Yang L, Liu C, Jiang L, Liu G, Liu P, Luo L (2023) Multi-omics-based identification of purple acid phosphatases and metabolites involved in phosphorus recycling in stylo root exudates. Int J Biol Macromol 241:124569

    Article  CAS  PubMed  Google Scholar 

  • Xia ZC, Kong CH, Chen LC, Wang P, Wang SL (2016) A broadleaf species enhances an autotoxic conifers growth through belowground chemical interactions. Ecology 97:2283–2292

    Article  PubMed  Google Scholar 

  • Xiang G, Ma W, Gao S, Jin Z, Yue Q, Yao Y (2019) Transcriptomic and phosphoproteomic profiling and metabolite analyses reveal the mechanism of NaHCO3-induced organic acid secretion in grapevine roots. BMC Plant Biol 19:383

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie T, Gu W, Wang M, Zhang L, Li C, Li C, Li W, Li L (2019) Exogenous 2-(3,4-dichlorophenoxy) triethylamine ameliorates the soil drought effect on nitrogen metabolism in maize during the pre-female inflorescence emergence stage. BMC Plant Biol 19:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie E, Wei X, Ding A, Zheng L, Wu X, Anderson B (2020) Short-term effects of salt stress on the amino acids of Phragmites australis root exudates in constructed wetlands. Water 12(2):569. https://doi.org/10.3390/w12020569

    Article  CAS  Google Scholar 

  • Xiong D, Huang J, Lin TC, Liu X, Xu C, Chen S, Yang Z, Chen G, Yang Y (2023) Warming increased metabolite composition and pathways in root exudates of chinese fir saplings in subtropical China. J Soil Sci Plant Nutr 23:2545–2565. https://doi.org/10.1007/s42729-023-01212-8

    Article  CAS  Google Scholar 

  • Xu K, Lee YS, Li J, Li C (2019) Resistance mechanisms and reprogramming of microorganisms for efficient bio-refinery under multiple environmental stresses. Synth Syst Biotechnol 4:92–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Yang M, Yin R, Wang L, Luo L, Zi B et al (2021) Autotoxin Rg1 induces degradation of root cell walls and aggravates root rot by modifying the rhizospheric microbiome. Microbiol Spectr 9:e0167921. https://doi.org/10.1128/spectrum.01679-21

    Article  PubMed  Google Scholar 

  • Yang NJ, Hinner MJ (2015) Getting across the cell membrane: an overview for small molecules, peptides, and proteins. In: Gautier A, Hinner M (eds) Site-specific protein labelling: methods in molecular biology. Humana Press, New York

    Google Scholar 

  • Yang Y, Yang Z, Yu S, Chen H (2019) Organic acids exuded from roots increase the available potassium content in the rhizosphere soil: a rhizobag experiment in Nicotiana tabacum. Hort Sci 54:23–27

    CAS  Google Scholar 

  • Yang S, Liu H, Xie P, Wen T, Shen Q, Yuan J (2023) Emerging pathways for engineering the rhizosphere microbiome for optimal plant health. J Agric Food Chem 71:4441–4449. https://doi.org/10.1021/acs.jafc.2c08758

    Article  CAS  PubMed  Google Scholar 

  • Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307

    Article  CAS  PubMed  Google Scholar 

  • Yildirim E, Taylor AG, Spittler TD (2006) Ameliorative effects of biological treatments on growth of squash plants under salt stress. Sci Hortic 111:1–6

    Article  CAS  Google Scholar 

  • Yin S, Wang C, Lv C, Zhou Z (2023) Short-term responses of root traits and carbon exudation to drought in a Larix gmelinii plantation. Plant Soil 484:393–405. https://doi.org/10.1007/s11104-022-05800-y

    Article  CAS  Google Scholar 

  • Yuan J, Zhao J, Wen T et al (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156. https://doi.org/10.1186/s40168-018-0537-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan T, Ren W, Wang Z, Fry EL, Tang S, Yin J, Zhang J, Jia Z (2023) How does the pattern of root metabolites regulating beneficial microorganisms change with different grazing pressures? Front Plant Sci 14:1180576. https://doi.org/10.3389/fpls.2023.1180576

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, Cho H, Karaoz U (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Vivanco JM, Shen Q (2017) The unseen rhizosphere root–soil–microbe interactions for crop production. Curr Opin Microbiol 37:8–14

    Article  PubMed  Google Scholar 

  • Zhang DS, Lyu Y, Li HB, Tang XY, Hu R, Rengel Z, Zhang FS, Whalley WR, Davies W, Cahill JF Jr, Shen JB (2020) Neighbouring plants modify maize root foraging for phosphorus: coupling nutrients and neighbours for improved nutrient-use efficiency. New Phytol 226(1):244–253

    Article  PubMed  Google Scholar 

  • Zhang W, Gao W, Whalley WR, Ren T (2021) Physical properties of a sandy soil as affected by incubation with a synthetic root exudate: strength, thermal and hydraulic conductivity, and evaporation. J Soil Sci 72:782–792

    Article  CAS  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  CAS  PubMed  Google Scholar 

  • Zhao M, Zhao J, Yuan J, Hale L, Wen T, Huang Q, Vivanco JM, Zhou J (2021a) Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth. Plant Cell Environ 44:613–628

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021b) Regulation of plant responses to salt stress. Int J Mol Sci 22(9):4609. https://doi.org/10.3390/ijms22094609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou C, Guo J, Zhu L, Xiao X, Xie Y, Zhu J, Ma Z, Wang J (2016) Paenibacillus polymyxa BFKC01 enhances plant iron absorption via improved root systems and activated iron acquisition mechanisms. Plant Physiol Biochem 105:162–173

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Wang Q, Liu W, Li B, Shao M, Zhang Y (2022) Effects of red/blue versus white LED light of different intensities on the growth and organic carbon and autotoxin secretion of hydroponic lettuce. Hortic Environ Biotechnol 63:195–205. https://doi.org/10.1007/s13580-021-00394-3

    Article  CAS  Google Scholar 

  • Zhou X, Zhang J, Urahman MK, Gao D, Wei Z, Wu F, Dini-Andreote F (2023a) Interspecific plant interaction via root exudates structures the disease suppressiveness of rhizosphere microbiomes. Mol Plant 16(5):849–864. https://doi.org/10.1016/j.molp.2023.03.009

    Article  CAS  PubMed  Google Scholar 

  • Zhou XG, Zhang JY, Rahman MKU, Gao DM, Wei Z, Wu FZ et al (2023b) Interspecific plant interaction via root exudates structures the disease suppressiveness of rhizosphere microbiomes. Mol Plant 16:849–864. https://doi.org/10.1016/j.molp.2023.03.009

    Article  CAS  PubMed  Google Scholar 

  • Zimmer W, Kloos K, Hundeshagen B, Niederau E, Bothe H (1995) Auxin biosynthesis and denitrification in plant growth promoting bacteria. In: Fendrik I, Del Gallo M, Vanderleyden J, de Zamaroczy M (eds) Azospirillum VI and related microorganisms, genetics-physiology-ecology. Springer, Berlin, pp 121–128

    Chapter  Google Scholar 

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Funding

The work is funded by Science and Engineering Research Board, Dept. of Science and Technology, Govt. of India via sanction order CRG/2019/000414 dated 27th January 2020.

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OPA: Conceptualization, drafting and editing; DY: Drafting, figures making; NW: Reference setting and editing PLK: Drafting and editing; PS: Editing and RT: Editing.

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Ahlawat, O.P., Yadav, D., Walia, N. et al. Root Exudates and Their Significance in Abiotic Stress Amelioration in Plants: A Review. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11237-7

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