Abstract
Plant roots secrete various organic substances into the rhizosphere, which are a source of nutrition for microorganisms and largely determine the nature of plant–microbe interactions. The composition of the main fractions of root exudates in ten modern varieties of wheat was determined: the contents of amino acids, organic acids, and sugars were analyzed. Reliable qualitative and quantitative differences between varieties for individual components of exudates were revealed, which determined the peculiarities of cultivar clustering on this trait. Relationships between exudation and the effectiveness of plant interaction with the growth-promoting rhizobacterium Pseudomonas fluorescens SPB2137 and the phytopathogenic fungus Fusarium culmorum 30 in laboratory systems, as well as with the resistance of the varieties to diseases in the field, were found. The number of P. fluorescens SPB2137 in the root zone positively correlated with the amounts of many amino acids, as well as maltose, secreted by the roots. The stimulating effect of rhizobacteria on root growth positively correlated with the amount of released glucose and melibiose. A relationship between the nature of root exudation and root colonization or the susceptibility of the varieties to F. culmorum 30 was not found. An analysis of the correlations between the incidence of wheat varieties in the field and the intensity of exudation of certain substances, as well as with the biocomposition index of amino acid exudation, was carried out. The role of root exudate components in the formation of effective plant-microbial systems is discussed.
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REFERENCES
Byerlee, D. and Moya, P., Impacts of International Wheat Breeding Research in the Developing World, 1966–1990, Heisey, P.W., Lantican, M.A., and Dubin, H.J., Eds., Mexico: International Maize and Wheat Improvement Center (CIMMYT), D.F., 1993.
Pingali, P., Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, no. 31, pp. 12302–12308.
Raeboline, A., Nelson, L.E., Ravichandran, K., and Antony, U., J. Ethnic Foods, 2019, vol. 6, p. 8. https://doi.org/10.1186/s42779-019-0011-9
Pearce, S., J. Exp. Bot., 2021, vol. 72, no. 2, pp. 157–160.
Sharma, R.C., Morgounov, A., Akin, B., Bespalova, L., Lang, L., Litvinenko, M., et al., Crop Sci., 2014, vol. 54, no. 6, pp. 2469–2480.
Li, S., Zhang, C., Li, J., Yan, L., Wang, N., and Xia, L., Plant Commun., 2021, vol. 2, no. 4, p. 100211.
Elkoca, E., Turan, M., and Donmez, M.F., J. Plant Nutr., 2010, vol. 33, pp. 2104–2119.
Vessey, J.K., Plant Soil, 2003, vol. 255, pp. 571–586.
Ryan, P.R., Dessaux, Y., Thomashow, L.S., and Weller, D.M., Plant Soil, 2009, vol. 321, pp. 363–383.
Kozhemyakov, A.P., Belobrova, S.N., and Orlova, A.G., S.-kh. Biol., 2011, no. 3, pp. 112–115.
Chandran, H., Meena, M., and Swapnil, P., Sustainability, 2021, vol. 13, p. 10986. https://doi.org/10.3390/su131910986
Beneduzi, A., Ambrosini, A., and Passaglia, L.M.P., Genet. Mol. Biol., 2012, vol. 35, pp. 1044–1051.
Chaluvadi, S. and Bennetzen, J.L., Front. Plant Sci, 2018, vol. 9, p.1183. https://doi.org/10.3389/fpls.2018.01183
Kudoyarova, G., Arkhipova, T., Korshunova, T., Bakaeva, M., Loginov, O., and Dodd, I.C., Front. Plant Sci., 2019, vol. 10, p. 1368.https://doi.org/10.3389/fpls.2019.01368
Mohanram, S. and Kumar, P., Ann. Microbiol., 2019, vol. 69, pp. 307–320.
Weller, D.M. and Thomashow, L.S., in Molecular Ecology of Rhizosphere Microorganisms, O’Gara, F., Dowling, D.N., and Boesten, B., Eds., Weinheim: VCH Publisher Inc., 1994, pp. 1–18.
Whipps, J.M., J. Exp. Bot., 2001, vol. 52, pp. 487–511.
Belimov, A., Kojemiakov, A., and Chuvarliyeva, C., Plant Soil, 1995, vol. 173, pp. 29–37.
Lugtenberg, B. and Kamilova, F., Annu. Rev. Microbiol., 2009, vol. 63, pp. 541–556.
Burgmann, H., Meier, S., Bunge, M., Widmer, F., and Zeyer, J., Environ. Microbiol., 2005, vol. 7, pp. 1711–1724.
Lugtenberg, B.J.J., Dekkers, L., and Bloemberg, G.V., Annu. Rev. Phytopathol., 2001, vol. 39, pp. 461–490.
Kravchenko, L.V., Azarova, T.S., Leonova-Erko, E.I., Shaposhnikov, A.I., Makarova, N.M., and Tikhonovich, I.A., Microbiology (Moscow), 2003, vol. 72, no. 1, pp. 37–41.
de Werra, P., Huser, A., Tabacchi, R., Keel, C., and Maurhofer, M., Appl. Environ. Microbiol., 2011, vol. 77, no. 8, pp. 2807–2812.
Lynch, J.M. and Whipps, J.M., Plant Soil, 1990, vol. 129, pp. 1–10.
Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M., Ann. Rev. Plant Biol., 2006, vol. 57, pp. 233–266.
de Weert, S., Vermeiren, H., Mulders, I.H.M., Kuiper, I., Hendrickx, N., Bloemberg, G.V., Vanderleyden, J., De Mot, R., and Lugtenberg, B.J.J., Mol. Plant–Microbe Interact., 2002, vol. 15, pp. 1173–1180.
Rudrappa, T., Czymmek, K.J., Pare, P.W., and Bais, H.P., Plant Physiol., 2008, vol. 148, pp. 1547–1556.
Ling, N., Raza, W., Ma, J., Huang, Q., and Shen, Q., Eur. J. Soil Biol., 2011, vol. 47, pp. 374–379.
Tan, S., Yang, C., Mei, X., Shen, S., Raza, W., Shen, Q., and Xu, Y., Appl. Soil. Ecol., 2013, vol. 64, pp. 15–22.
Ren, L., Huo, H., Zhang, F., Hao, W., Xiao, L., Dong, C., and Xu, G., Plant Signal. Behav., 2016, vol. 11, no. 6, p. e1187357. https://doi.org/10.1080/15592324.2016.1187357
Perry, L.G., Alford, E.R., Horiuchi, J., Paschke, M., and Vivanco, J.M., in The Rhizosphere, Pinton, R., Varanini, Z., and Nannipieri, P., Eds., Boca Raton, FL: CRC, 2007, 2nd ed., pp. 297–330.
Broeckling, C.D., Broz, A.K., Bergelson, J., Manter, D.K., and Vivanco, J.M., Appl. Environ. Microbiol., 2008, vol. 74, no. 3, pp. 738–744.
Kravchenko, L.V., Shaposhnikov, A.I., Makarova, N.M., Azarova, T.S., L’vova, K.A., Kostyuk, I.I., Lyapunova, O.A., and Tikhonovich, I.A., Russ. J. Plant Physiol., 2011, vol. 58, no. 5, pp. 936–940.
Stringlis, I.A., Yu, K., Feussner, K., de Jonge, R., Van Bentum, S., Van Verk, M.C., Berendsen, R.L., Bakker, P.A.H.M., Feussner, I., and Pieterse, C.M.J., Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, no. 22, pp. E5213–E5222.
Cotton, T.E.A., Pe’triacq, P., Cameron, D.D., Meselmani, M.A., Schwarzenbacher, R., Rolfe, S.A., and Ton, J., ISME J., 2019, vol. 13, pp. 1647–1658.
Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B., Goossens, A., Nutzmann, H.W., Bai, Y., and Osbourn, A., Science, 2019, vol. 364, no. 6440, p. eaau6389. https://doi.org/10.1126/science.aau6389
Prudence, S.M., Newitt, J.T., Worsley, S.F., Macey, M.C., Murrell, J.C., Lehtovirta-Morley, L.E., and Hutchings, M.I., Environ. Microbiome, 2021, vol. 16, p. 12. https://doi.org/10.1186/s40793-021-00381-2
Shi, J.B., Gong, X.Y., Khashi u Rahman, M., Tian, Q., Zhou, X.G., and Wu, F.Z., Plant Soil Environ., 2021, vol. 67, pp. 721–728.
Owens, A.G. and Jones, D.L., Soil Biol. Biochem., 2001, vol. 33, pp. 651–657.
Chen, S., Waghmode, T.R., Sun, R., Kuramae, E.E., Hu, C., and Liu, B., Microbiome, 2019, vol. 7, p. 136. https://doi.org/10.1186/s40168-019-0750-2
Hu, L., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A., Schlaeppi, K., and Erb, M., Nat. Commun., 2018, vol. 9, p. 2738. https://doi.org/10.1038/s41467-018-05122-7
Belimov, A.A., Dodd, I.C., Safronova, V.I., Shaposhnikov, A.I., Azarova, T.S., Makarova, N.M., Davies, W.J., and Tikhonovich, I.A., Ann. Appl. Biol., 2015, vol. 167, pp. 11–25.
Phillips, D.A., Fox, T.C., King, M.D., Bhuvaneswari, T.V., and Teuber, L.R., Plant Physiol., 2004, vol. 136, pp. 2887–2894.
Kawasaki, A., Dennis, P.G., Forstner, C., Raghavendra, A.K.H., Mathesius, U., Richardson, A., Delhaize, E., Gilliham, M., Watt, M., and Ryan, P.R., Plant Physiol., 2021, vol. 187, pp. 2279–2295.
Yahya, M., Islam, E.U., Rasul, M., Farooq, I., Mahreen, N., Tawab, A., Irfan, M., Rajput, L., Amin, I., and Yasmin, S., Front. Microbiol., 2021, vol. 12, p. 744094. https://doi.org/10.3389/fmicb.2021.744094
Sasse, J., Martinoia, E., and Northen, T., Trends Plant Sci., 2018, vol. 25, no. 1, pp. 25–41.
Tsunoda, T. and van Dam, N.M., Pedobiologia, 2017, vol. 65, pp. 58–67.
Pang, Z., Chen, J., Wang, T., Gao, C., Li, Z., Guo, L., Xu, J., and Cheng, Y., Front. Plant Sci., 2021, vol. 12.
Kravchenko, L.V., Makarova, N.M., Azarova, T.S., Provorov, N.A., and Tikhonovich, I.A., Microbiology (Moscow), 2002, vol. 71, no. 4, pp. 444–448.
Strunnikova, O.K., Shakhnazarova, V.Yu., Vishnevskaya, N.A, Ruchii, A.S, and Chizhevskaya, E.P., Mikol. Fitopatol., 2013, vol. 47, no. 3, pp. 196–203.
Magurran, A.E., Ecological Diversity and Its Measurement, London: Chapman and Hall, 1983.
Gorodnichev, R.M., Pestryakova, L.A., Ushnitskaya, L.A., Levina, S.N., and Davydova, P.V., Metody ekologicheskikh issledovanii. Osnovy statisticheskoi obrabotki dannykh: uchebno-metodicheskoe posobie (Methods of Ecological Research. Fundamentals of Statistical Data Processing: Educational and Methodological Guide), Yakutsk: Izd. Dom SVFU, 2019.
Mandelbrot, B., Fraktal’naya geometriya prirody (Fractal Geometry of Nature), Moscow: Institut komp’yuternykh issledovanii, 2002.
Sergeev, A.P. and Tarasov, D.A., Vvedenie v neirosetevoe modelirovanie: uchebnoe plobie (Introduction to Neural Network Modeling: Tutorial), Yekaterinburg: Ural. Univ., 2017.
Gudfellou, Ya., Bendzhio, I., and Kurvill’, A., Glubokoe obuchenie (Deep Learning), Moscow: DMK Press, 2018.
Naher, U.A., Radziah, O., Halimi, M.S., Shamsuddin, Z.H., and Mohd Razi, I., Res. J. Microbiol., 2008, vol. 3, pp. 580–587.
Kuzmicheva, Yu.V., Shaposhnikov, A.I., Azarova, T.S., Petrova, S.N., Naumkina, T.S., Borisov, A.Yu., Belimov, A.A., et al., Russ. J. Plant Physiol., 2014, vol. 61, no. 1, pp. 112–118.
Inceoglu, Ö., Salles, J.F., and van Elsas, J.D., Microbiol. Ecol., 2012, vol. 63, pp. 460–470.
Kuzmicheva, Y.V., Shaposhnikov, A.I., Petrova, S.N., Makarova, N.M., Tychinskaya, I.L., Puhalsky, J.V., et al., Plant Soil, 2017, vol. 419, pp. 83–96.
Shaposhnikov, A.I., Morgunov, A., Akin, B., Makarova, N.M., Belimov, A.A., and Tikhonovich, I.A., S.-kh. Biol., 2016, vol. 51, no. 1, pp. 58–78.
Beleggia, R., Rau, D., Laidò, G., Platani, C., Nigro, F., Fragasso, M., De Vita, P., Scossa, F., Fernie, A.R., Nikoloski, Z., and Papa, R., Mol. Biol. Evol., 2016, vol. 33, pp. 1740–1753.
Iannucci, A., Fragasso, M., Beleggia, R., Nigro, F., and Papa, R., Front. Plant Sci., 2017, vol. 8, p. 2124. https://doi.org/10.3389/fpls.2017.02124
Qu, Q., Li, Y., Zhang, Z., Cui, H., Zhao, Q., Liu, W., Lu, T., and Qian, H., J. Hazard Mater., 2021, vol. 411, p. 125137. https://doi.org/10.1016/j.jhazmat.2021.125137
O’Neal, L., Vo, L., and Alexandre, G., Appl. Environ. Microbiol., 2020, vol. 86, no. 15, p. e01026-20. https://doi.org/10.1128/AEM.01026-20
Tsavkelova, E.A., Klimova, S.Yu., Cherdyntseva, T.A., and Netrusov, L.I., Appl. Biochem. Microbiol., 2006, vol. 42, no. 2, pp. 117–126.
Patten, C.L., Blakney, A.J., and Coulson, T.J., Crit. Rev. Microbiol., 2013, vol. 39, no. 4, pp. 395–415.
Syrova, D.S., Shaposhnikov, A.I., Yuzikhin, O.S., and Belimov, A.A., Appl. Biochem. Microbiol., 2022, vol. 58, no. 1, pp. 1–18.
Glick, B.R., Biljana, T., Czarny, J., Cheng, Z., Duan, J., and McConkey, B., Crit. Rev. Plant Sci., 2007, vol. 26, pp. 227–242.
Bogatykh, B.A., Fraktal’naya priroda zhivogo: sistemnoe issledovanie biologicheskoi evolyutsii i prirody soznaniya (The Fractal Nature of Living Things: A Systematic Study of Biological Evolution and the Nature of Consciousness), Moscow: LIBEKOM, 2012.
Mandelbrot, B., Fraktal’naya geometriya prirody (Fractal Geometry of Nature), Moscow: Institut komp’yuternykh issledovanii, 2002.
Gafarov, F.M. and Galimyanov, A.F., Iskusstvennye neironnye seti i prilozheniya: uchebnoe posobie (Artificial Neural Networks and Applications: Tutorial), Kazan: Kazan. Univ., 2018.
Vorob'ev, N.I. and Selina, M.V., Perm. Agrarn. Vestn., 2021, no. 4 (36), pp. 92–99.
Keller, B., Wicker, T., and Krattinger, S.G., Annu. Rev. Phytopathol., 2018, vol. 56, pp. 67–87.
Wulff, B.B. and Krattinger, S.G., Curr. Opin. Biotechnol., 2022, vol. 73, pp. 270–275.
Dracatos, P.M., Haghdoust, R., Singh, D., and Park, R.F., New Phytol., 2018, vol. 218, no. 2, pp. 453–462.
Provorov, N.A., Tikhonovich, I.A., and Vororb’ev, N.I., Russ. J. Genet., 2016, vol. 52, no. 2, pp. 117–124.
Rengel, Z., Plant Soil, 2002, vol. 245, pp. 59–70.
Wang, J., Li, R., Zhang, H., Wei, G., and Li, Z., BMC Microbiol., 2020, vol. 20, p. 38. https://doi.org/10.1186/s12866-020-1708-z
ACKNOWLEDGMENTS
The authors are grateful to P.S. Ulyanich (All-Russia Research Institute for Agricultural Microbiology) for constructing Fig. 4.
Funding
The work on plant cultivation and analysis of root exudates was supported financially by the Russian Foundation for Basic Research (project no. 15-04-09023). Mathematical and bioinformatics work was supported by the Russian Science Foundation (project no. 22-26-00341).
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Shaposhnikov, A.I., Belimov, A.A., Azarova, T.S. et al. The Relationship Between the Composition of Root Exudates and the Efficiency of Interaction of Wheat Plants with Microorganisms. Appl Biochem Microbiol 59, 330–343 (2023). https://doi.org/10.1134/S000368382303016X
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DOI: https://doi.org/10.1134/S000368382303016X