Microbe-assisted crop improvement: a sustainable weapon to restore holobiont functionality and resilience

Abstract

In the past years, breeding programs have been mainly addressed on pushing the commercial features, forgetting important traits, such as those related to environmental stress resilience, that are instead present in wild relatives. Among the traits neglected by breeding processes, the ability to recruit beneficial microorganisms that recently is receiving a growing attention due to its potentiality. In this context, this review will provide a spotlight on critical issues of the anthropocentric point of view that, until now, has characterized the selection of elite plant genotypes. Its effects on the plant-microbiome interactions, and the possibility to develop novel strategies mediated by the exploitation of beneficial root-microbe interactions, will be discussed. More sustainable microbial-assisted strategies might in fact foster the green revolution and the achievement of a more sustainable agriculture in a climatic change scenario.

References

[1] Agovino M, Casaccia M, Ciommi M et al. Agriculture, climate change and sustainability: the case of EU-28. Ecol Indic. 2019; 105: 525-43.

[2] Arora NK . Impact of climate change on agriculture production and its sustainable solutions. Environ Sustain. 2019; 2: 95-6.

[3] Elkerbout M, Egenhofer C, Núñez Ferrer J et al. The european green deal after corona: implications for eu climate policy. CEPS Policy Insights. 2020; 6: 1-12.

[4] Hickey LT, Hafeez AN, Robinson H et al. Breeding crops to feed 10 billion. Nat Biotechnol. 2019; 37: 744-54.

[5] Nerva L, Giudice G, Quiroga G et al. Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs. Biol Fertil Soils. 2021;58:17-34.

[6] Jacott CN, Murray JD, Ridout CJ . Trade-offs in arbuscular mycorrhizal Symbiosis: disease resistance, growth responses and perspectives for crop breeding. Agronomy. 2017; 7.

[7] Bastías DA, Gianoli E, Gundel PE . Fungal endophytes can eliminate the plant growth-defence trade-off. New Phytol. 2021; 230: 2105-13.

[8] Chen YH, Gols R, Benrey B . Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol. 2015; 60: 35-58.

[9] Matson PA, Parton WJ, Power AG et al. Agricultural intensification and ecosystem properties. Science. 1997; 277: 504-9.

[10] Gepts P . Crop Domestication as a Long-Term Selection Experiment. In: Janick J (ed.). Plant Breeding Reviews.Bridgewater, NJ: John Wiley & Sons, Ltd, 2003, 1-44.

[11] Babalola OO . Beneficial bacteria of agricultural importance. Biotechnol Lett. 2010; 32: 1559-70.

[12] Yadav AN, Mishra S, Kour D et al. Agriculturally Important Fungi for Sustainable Agriculture. Switzerland AG: Springer Nature; 2020.

[13] Gosling P, Hodge A, Goodlass G et al. Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ. 2006; 113: 17-35.

[14] Antoine S, Hériché M, Boussageon R et al. A historical perspective on mycorrhizal mutualism emphasizing arbuscular mycorrhizas and their emerging challenges. Mycorrhiza. 2021; 31: 637-53.

[15] Johansson JF, Paul LR, Finlay RD . Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol. 2004; 48: 1-13.

[16] Zeder MA . Core questions in domestication research. Proc Natl Acad Sci. 2015; 112: 3191-8.

[17] Hetrick B, Wilson G, Cox T . Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot. 1992; 70: 2032-40.

[18] Sangabriel-Conde W, Negrete-Yankelevich S, Maldonado-Mendoza IE et al. Native maize landraces from Los Tuxtlas, Mexico show varying mycorrhizal dependency for P uptake. Biol Fertil Soils. 2014; 50: 405-14.

[19] Lauber CL, Hamady M, Knight R et al. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol. 2009; 75: 5111-20.

[20] Zarraonaindia I, Owens SM, Weisenhorn P et al. The soil microbiome influences grapevine-associated microbiota. MBio. 2015; 6: e02527-14.

[21] Johnston-Monje D, Lundberg DS, Lazarovits G et al. Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil. 2016; 405: 337-55.

[22] Millán-Aguiñaga N, Soldatou S, Brozio S et al. Awakening ancient polar Actinobacteria: diversity, evolution and specialized metabolite potential. Microbiology. 2019; 165: 1169-80.

[23] Ramijan K, Ultee E, Willemse J et al. Stress-induced formation of cell wall-deficient cells in filamentous actinomycetes. Nat Commun. 2018; 9: 1-13.

[24] Choudhary DK, Johri BN . Interactions of bacillus spp. and plants-with special reference to induced systemic resistance (ISR). Microbiol Res. 2009; 164: 493-513.

[25] McSpadden Gardener BB . Diversity and ecology of biocontrol Pseudomonas spp. in agricultural systems. Phytopathology. 2007; 97: 221-6.

[26] Harman GE . Overview of mechanisms and uses of Trichoderma spp. Phytopathology. 2006; 96: 190-4.

[27] Kamal R, Gusain YS, Kumar V . Interaction and symbiosis of AM fungi, actinomycetes and plant growth promoting rhizobacteria with plants: strategies for the improvement of plants health and defense system. Int J Curr Microb Appl Sci. 2014; 3: 564-85.

[28] Lu H, Bian R, Xia X et al. Legacy of soil health improvement with carbon increase following one time amendment of biochar in a paddy soil - a rice farm trial. Geoderma. 2020; 376: 114567.

[29] Liu C, Xia R, Tang M et al. Improved ginseng production under continuous cropping through soil health reinforcement and rhizosphere microbial manipulation with biochar: a field study of Panax ginseng from Northeast China. Hort Res. 2022; 9: uhac108.

[30] Vandenkoornhuyse P, Quaiser A, Duhamel M et al. The importance of the microbiome of the plant holobiont. New Phytol. 2015; 206: 1196-206.

[31] Singh BK, Trivedi P, Egidi E et al. Crop microbiome and sustainable agriculture. Nat Rev Microbiol. 2020; 18: 601-2.

[32] Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol. 2009; 84: 11-8.

[33] Martínez-Romero E, Aguirre-Noyola JL, Taco-Taype N et al. Plant microbiota modified by plant domestication. Syst Appl Microbiol. 2020; 43: 126106.

[34] Smýkal P, Nelson MN, Berger JD et al. The impact of genetic changes during crop domestication. Agronomy. 2018; 8: 119.

[35] Stuthman D, Leonard K, Miller-Garvin J . Breeding crops for durable resistance to disease. Adv Agron. 2007; 95: 319-67.

[36] Nelson R, Wiesner-Hanks T, Wisser R et al. Navigating complexity to breed disease-resistant crops. Nat Rev Genet. 2018; 19: 21-33.

[37] Fonseca JP, Mysore KS . Genes involved in nonhost disease resistance as a key to engineer durable resistance in crops. Plant Sci. 2019; 279: 108-16.

[38] Prasanna H, Sinha D, Rai G et al. Pyramiding Ty-2 and Ty-3 genes for resistance to monopartite and bipartite tomato leaf curl viruses of India. Plant Pathol. 2015; 64: 256-64.

[39] Qu S, Liu G, Zhou B et al. The broad-Spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in Rice. Genetics. 2006; 172: 1901-14.

[40] Harshman JM, Evans KM, Hardner CM . Cost and accuracy of advanced breeding trial designs in apple. Hortic Res. 2016; 3: 16008.

[41] Limera C, Sabbadini S, Sweet JB et al. New biotechnological tools for the genetic improvement of major Woody fruit species. Front Plant Sci. 2017; 8: 1418.

[42] Ricci A, Sabbadini S, Prieto H et al. Genetic transformation in peach (Prunus persica L.): challenges and ways forward. Plan Theory. 2020; 9: 971.

[43] Krishnan HB, Jez JM . Review: the promise and limits for enhancing sulfur-containing amino acid content of soybean seed. Plant Sci. 2018; 272: 14-21.

[44] Carbonell-Bejerano P, Royo C, Mauri N, Ibáñez J, Miguel Martínez Zapater J . Somatic Variation and Cultivar Innovation in Grapevine. In: Morata A, Loira I (eds). Advances in Grape and Wine Biotechnology.London, UK: IntechOpen, 2019.

[45] Eibach R, Töpfer R . Traditional grapevine breeding techniques. In: Reynolds A (eds). Grapevine Breeding Programs for the Wine Industry.London, UK: Elsevier Woodhead Publishing, 2015, 3-22.

[46] Massel K, Lam Y, Wong ACS et al. Hotter, drier, CRISPR: the latest edit on climate change. Theor Appl Genet. 2021; 134: 1691-709.

[47] Giudice G, Moffa L, Varotto S et al. Novel and emerging biotechnological crop protection approaches. Plant Biotechnol J. 2021; 19: 1495-510.

[48] Biswas S, Zhang D, Shi J . CRISPR/Cas systems: opportunities and challenges for crop breeding. Plant Cell Rep. 2021; 40: 979-98.

[49] Zhang D, Hussain A, Manghwar H et al. Genome editing with the CRISPR-Cas system: an art, ethics and global regulatory perspective. Plant Biotechnol J. 2020; 18: 1651-69.

[50] Gonzalez Guzman M, Cellini F, Fotopoulos V et al. New approaches to improve crop tolerance to biotic and abiotic stresses. Physiol Plant. 2022; 174: e13547.

[51] Leung K, Ras E, Ferguson KB et al. Next-generation biological control: the need for integrating genetics and genomics. Biol Rev. 2020; 95: 1838-54.

[52] Silva-Valderrama I, Toapanta D, Miccono MA et al. Biocontrol potential of grapevine endophytic and rhizospheric fungi against trunk pathogens. Front Microbiol. 2021; 11: 3311.

[53] Nigris S, Baldan E, Tondello A et al. Biocontrol traits of bacillus licheniformis GL174, a culturable endophyte of Vitis vinifera cv. Glera. BMC Microbiol. 2018; 18: 1-16.

[54] Andreolli M, Lampis S, Zapparoli G et al. Diversity of bacterial endophytes in 3 and 15 year-old grapevines of Vitis vinifera cv. Corvina and their potential for plant growth promotion and phytopathogen control. Microbiol Res. 2016; 183: 42-52.

[55] Cai X-C, Liu C-H, Wang B-T et al. Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiol Res. 2017; 196: 89-94.

[56] Palmieri D, Vitale S, Lima G et al. A bacterial endophyte exploits chemotropism of a fungal pathogen for plant colonization. Nat Commun. 2020; 11: 1-11.

[57] Wei Z, Jousset A . Plant breeding goes microbial. Trends Plant Sci. 2017; 22: 555-8.

[58] Berendsen RL, Pieterse CM, Bakker PA . The rhizosphere microbiome and plant health. Trends Plant Sci. 2012; 17: 478-86.

[59] Zancarini A, Westerhuis JA, Smilde AK et al. Integration of omics data to unravel root microbiome recruitment. Curr Opin Biotechnol. 2021; 70: 255-61.

[60] Tian B, Pei Y, Huang W et al. Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant. ISME J. 2021; 15: 1919-30.

[61] Rolfe SA, Griffiths J, Ton J . Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes. Curr Opin Microbiol. 2019; 49: 73-82.

[62] Sandrini M, Nerva L, Sillo F et al. Abiotic stress and belowground microbiome: the potential of omics approaches. Int J Mol Sci. 2022; 23: 1091.

[63] Berendsen RL, Vismans G, Yu K et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 2018; 12: 1496-507.

[64] Bakker MG, Manter DK, Sheflin AM et al. Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil. 2012; 360: 1-13.

[65] Lapsansky ER, Milroy AM, Andales MJ et al. Soil memory as a potential mechanism for encouraging sustainable plant health and productivity. Curr Opin Biotechnol. 2016; 38: 137-42.

[66] Hannula SE, Heinen R, Huberty M et al. Persistence of plant-mediated microbial soil legacy effects in soil and inside roots. Nat Commun. 2021; 12: 5686.

[67] Van Der Heijden MG, Hartmann M . Networking in the plant microbiome. PLoS Biol. 2016; 14: e1002378.

[68] Lynch JP . Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol. 2019; 223: 548-64.

[69] York LM, Carminati A, Mooney SJ et al. The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots. J Exp Bot. 2016; 67: 3629-43.

[70] de la Fuente CC, Simonin M, King E et al. An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. Plant J. 2020; 103: 951-64.

[71] Herms CH, Hennessy RC, Bak F et al. Back to our roots: exploring the role of root morphology as a mediator of beneficial plant-microbe interactions. Environ Microbiol. 2022.

[72] Ober ES, Alahmad S, Cockram J et al. Wheat root systems as a breeding target for climate resilience. Theor Appl Genet. 2021; 134: 1645-62.

[73] Bardgett RD, Mommer L, De Vries FT . Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol. 2014; 29: 692-9.

[74] Grover M, Bodhankar S, Sharma A et al. PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst. 2021; 4: 287.

[75] Cataldi MP, Heuer S, Mauchline TH et al. Effect of plant growth promoting bacteria on the growth of wheat seedlings subjected to phosphate starvation. Agronomy. 2020; 10: 978.

[76] Araujo FF, Bonifacio A, Bavaresco LG et al. Bacillus subtilis changes the root architecture of soybean grown on nutrient-poor substrate. Rhizosphere. 2021; 18: 100348.

[77] Verma SK, Kingsley K, Bergen M et al. Bacterial endophytes from rice cut grass (Leersia oryzoides L.) increase growth, promote root gravitropic response, stimulate root hair formation, and protect rice seedlings from disease. Plant Soil. 2018; 422: 223-38.

[78] Rêgo MCF, Ilkiu-Borges F, de Filippi MCC et al. Morphoanatomical and biochemical changes in the roots of rice plants induced by plant growth-promoting microorganisms. Embrapa Arroz E Feijão-Artigo Em Periód Indexado ALICE. 2014; 2014: 1-10.

[79] Liu X, Jiang X, He X et al. Phosphate-solubilizing Pseudomonas sp. strain P34-L promotes wheat growth by colonizing the wheat rhizosphere and improving the wheat root system and soil phosphorus nutritional status. J Plant Growth Regul. 2019; 38: 1314-24.

[80] Wang E, Schornack S, Marsh JF et al. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol. 2012; 22: 2242-6.

[81] Sasse J, Martinoia E, Northen T . Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018; 23: 25-41.

[82] Eisenhauer N, Dobies T, Cesarz S et al. Plant diversity effects on soil food webs are stronger than those of elevated CO₂ and N deposition in a long-term grassland experiment . Proc Natl Acad Sci. 2013; 110: 6889-94.

[83] Prober SM, Leff JW, Bates ST et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett. 2015; 18: 85-95.

[84] Steinauer K, Chatzinotas A, Eisenhauer N . Root exudate cocktails: the link between plant diversity and soil microorganisms? Ecol Evol. 2016; 6: 7387-96.

[85] Hallama M, Pekrun C, Lambers H et al. Hidden miners-the roles of cover crops and soil microorganisms in phosphorus cycling through agroecosystems. Plant Soil. 2019; 434: 7-45.

[86] Kim N, Zabaloy MC, Guan K et al. Do cover crops benefit soil microbiome? A meta-analysis of current research. Soil Biol Biochem. 2020; 142: 107701.

[87] Gyssels G, Poesen J, Bochet E et al. Impact of plant roots on the resistance of soils to erosion by water: a review. Prog Phys Geogr. 2005; 29: 189-217.

[88] Chen G, Weil RR . Root growth and yield of maize as affected by soil compaction and cover crops. Soil Tillage Res. 2011; 117: 17-27.

[89] Han E, Kautz T, Perkons U et al. Quantification of soil biopore density after perennial fodder cropping. Plant Soil. 2015; 394: 73-85.

[90] Brady NC, Weil RR . The nature and properties of soils. Upper Saddle River. 2002.

[91] Tiemann L, Grandy A, Atkinson E et al. Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol Lett. 2015;18:761-71.

[92] Griffiths M, Delory BM, Jawahir V et al. Optimisation of root traits to provide enhanced ecosystem services in agricultural systems: a focus on cover crops. Plant Cell Environ. 2022; 45: 751-70.

[93] Xu L, Pierroz G, Wipf HML et al. Holo-omics for deciphering plant-microbiome interactions. Microbiome. 2021; 9: 1-11.

[94] Nerva L, Garcia JF, Favaretto F et al. The hidden world within plants: metatranscriptomics unveils the complexity of wood microbiomes. J Exp Bot. 2022; 73: 2682-97.

[95] Corbin KR, Bolt B, Rodríguez López CM . Breeding for beneficial microbial communities using epigenomics. Front Microbiol. 2020; 11: 937.

[96] Huang AC, Jiang T, Liu Y-X et al. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science. 2019; 364: eaau6389.

[97] Bulgarelli D, Schlaeppi K, Spaepen S et al. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol. 2013; 64: 807-38.

[98] Wang X, Wang M, Xie X et al. An amplification-selection model for quantified rhizosphere microbiota assembly. Sci Bull. 2020; 65: 983-6.

[99] Zolti A, Green SJ, Sela N et al. The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts. Microbiome. 2020; 8: 1-18.

[100] Li X, Jousset A, de Boer W et al. Legacy of land use history determines reprogramming of plant physiology by soil microbiome. ISME J. 2019; 13: 738-51.

[101] Toju H, Peay KG, Yamamichi M et al. Core microbiomes for sustainable agroecosystems. Nat Plants. 2018; 4: 247-57.

[102] Großkopf T, Soyer OS . Synthetic microbial communities. Curr Opin Microbiol. 2014; 18: 72-7.

[103] Carlström CI, Field CM, Bortfeld-Miller M et al. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat Ecol Evol. 2019; 3: 1445-54.

[104] Zhuang L, Li Y, Wang Z et al. Synthetic community with six pseudomonas strains screened from garlic rhizosphere microbiome promotes plant growth. Microb Biotechnol. 2021; 14: 488-502.

[105] Simonin M, Dasilva C, Terzi V et al. Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils. FEMS Microbiol Ecol. 2020; 96: fiaa067.

[106] Herrera Paredes S, Gao T, Law TF et al. Design of synthetic bacterial communities for predictable plant phenotypes. PLoS Biol. 2018; 16: e2003962.

[107] Ownley BH, Duffy BK, Weller DM . Identification and manipulation of soil properties to improve the biological control performance of phenazine-producing Pseudomonas fluorescens. Appl Environ Microbiol. 2003; 69: 3333-43.

[108] Rodriguez PA, Rothballer M, Chowdhury SP et al. Systems biology of plant-microbiome interactions. Mol Plant. 2019; 12: 804-21.

[109] Wintermans PC, Bakker PA, Pieterse CM . Natural genetic variation in Arabidopsis for responsiveness to plant growth-promoting rhizobacteria. Plant Mol Biol. 2016; 90: 623-34.

[110] Kroll S, Agler MT, Kemen E . Genomic dissection of host-microbe and microbe-microbe interactions for advanced plant breeding. Curr Opin Plant Biol. 2017; 36: 71-8.

[111] Du J, Li Y, Yin Z et al. High-throughput customization of plant microbiomes for sustainable agriculture. Front Plant Sci. 2020; 11: 1365.

[112] Costa C, Schurr U, Loreto F et al. Plant phenotyping research trends, a science mapping approach. Front Plant Sci. 2019; 9: 1933.

[113] Berg G, Rybakova D, Fischer D et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome. 2020; 8: 1-22.

[114] Nimnoi P, Pongsilp N, Lumyong S . Endophytic actinomycetes isolated from Aquilaria crassna Pierre ex Lec and screening of plant growth promoters production. World J Microbiol Biotechnol. 2010; 26: 193-203.

[115] Awasthi A . Field-specific microbial consortia are feasible: a response to Kaminsky et al. Trends Biotechnol. 2019; 37: 569-72.

[116] Schlaeppi K, Bulgarelli D . The plant microbiome at work. Mol Plant-Microbe Interact. 2015; 28: 212-7.

[117] Pérez-Jaramillo JE, Carrión VJ, Bosse M et al. Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J. 2017; 11: 2244-57.

[118] Pérez-Jaramillo JE, Carrión VJ, de Hollander M et al. The wild side of plant microbiomes. Microbiome. 2018; 6: 1-6.

[119] Gopal M, Gupta A, Thomas GV . Bespoke microbiome therapy to manage plant diseases. Front Microbiol. 2013; 4: 355.

[120] Klein E, Ofek M, Katan J et al. Soil suppressiveness to Fusarium disease: shifts in root microbiome associated with reduction of pathogen root colonization. Phytopathology. 2013; 103: 23-33.

[121] Aeron A, Khare E, Jha CK et al. Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future. Arch Microbiol. 2020; 202: 665-76.

[122] Bakker PA, Pieterse CM, Van Loon L . Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology. 2007; 97: 239-43.

[123] Kloepper JW, Ryu C-M, Zhang S . Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology. 2004; 94: 1259-66.

[124] David BV, Chandrasehar G, Selvam PN . Pseudomonas fluorescens: a plant-growth-promoting rhizobacterium (PGPR) with potential role in biocontrol of pests of crops. In: Prasad R, Gill SS, Tuteja N (eds). Crop Improvement through Microbial Biotechnology.London, UK: Elsevier, 2018, 221-43.

[125] Armada E, Probanza A, Roldán A et al. Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. J Plant Physiol. 2016; 192: 1-12.

[126] Ali SZ, Sandhya V, Grover M et al. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils. 2009; 46: 45-55.

[127] Kang S-M, Khan AL, Waqas M et al. Integrated phytohormone production by the plant growth-promoting rhizobacterium bacillus tequilensis SSB07 induced thermotolerance in soybean. J Plant Interact. 2019; 14: 416-23.

[128] Prudent M, Salon C, Souleimanov A et al. Soybean is less impacted by water stress using Bradyrhizobium japonicum and thuricin-17 from bacillus thuringiensis. Agron Sustain Dev. 2015; 35: 749-57.

[129] Chu TN, Tran BTH, Van Bui L et al. Plant growth-promoting rhizobacterium pseudomonas PS01 induces salt tolerance in Arabidopsis thaliana. BMC Res Notes. 2019; 12: 1-7.

[130] Karthika S, Midhun SJ, Jisha M . A potential antifungal and growth-promoting bacterium Bacillus sp. KTMA4 from tomato rhizosphere. Microb Pathog. 2020; 142: 104049.

[131] Noori MS, Saud HM . Potential plant growth-promoting activity of Pseudomonas sp. isolated from paddy soil in Malaysia as biocontrol agent. J Plant Pathol Microbiol. 2012; 3: 1-4.

[132] Millán-Aguiñaga N, Soldatou S, Brozio S et al. Awakening ancient polar Actinobacteria: diversity, evolution and specialized metabolite potential. Microbiology. 2019; 165: 1169-80.

[133] Ramijan K, Ultee E, Willemse J et al. Stress-induced formation of cell wall-deficient cells in filamentous actinomycetes. Nat Commun. 2018; 9: 1-13.

[134] Sprusansky O, Stirrett K, Skinner D et al. The bkdR gene of Streptomyces coelicolor is required for morphogenesis and antibiotic production and encodes a transcriptional regulator of a branched-chain amino acid dehydrogenase complex. J Bacteriol. 2005; 187: 664-71.

[135] Jeffrey L, Sahilah A, Son R et al. Isolation and screening of actinomycetes from Malaysian soil for their enzymatic and antimicrobial activities. J Trop Agric Food Sci. 2007; 35: 159.

[136] Oskay AM, Üsame T, Cem A . Antibacterial activity of some actinomycetes isolated from farming soils of Turkey. Afr J Biotechnol. 2004; 3: 441-6.

[137] Marappa N, Ramachandran L, Dharumadurai D et al. Plant growth-promoting active metabolites from Frankia spp. of actinorhizal casuarina spp. Appl Biochem Biotechnol. 2020; 191: 74-91.

[138] Van der Meij A, Worsley SF, Hutchings MI et al. Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev. 2017; 41: 392-416.

[139] Bhatti AA, Haq S, Bhat RA . Actinomycetes benefaction role in soil and plant health. Microb Pathog. 2017; 111: 458-67.

[140] Chukwuneme CF, Babalola OO, Kutu FR et al. Characterization of actinomycetes isolates for plant growth promoting traits and their effects on drought tolerance in maize. J Plant Interact. 2020; 15: 93-105.

[141] Segaran G, Sundar RDV, Settu S et al. A review on endophytic actinomycetes and their applications. J Chem Pharm Res. 2017; 9: 152-8.

[142] Sathya A, Vijayabharathi R, Gopalakrishnan S . Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech. 2017; 7: 1-10.

[143] Kim K, Yim W, Trivedi P et al. Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.). Plant Soil. 2010; 327: 429-40.

[144] Loqman S, Barka EA, Clément C et al. Antagonistic actinomycetes from Moroccan soil to control the grapevine gray mold. World J Microbiol Biotechnol. 2009; 25: 81-91.

[145] Gangwar M, Rani S, Sharma N . Investigating endophytic actinomycetes diversity from rice for plant growth promoting and antifungal activity. Int J Adv Life Sci IJALS. 2012; 1: 10-21.

[146] Wan M, Li G, Zhang J et al. Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control. 2008; 46: 552-9.

[147] Mhlongo MI, Piater LA, Madala NE et al. The chemistry of plant-microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci. 2018; 9: 112.

[148] Zothanpuia AKP, Yadav MK, Singh BP . In vitro evaluation of antimicrobial activities and antibiotic susceptibility profiling of culturable actinobacteria from fresh water streams. Indian J Exp Biol. 2018; 56: 665-73.

[149] Grover M, Bodhankar S, Maheswari M et al. Actinomycetes as mitigators of climate change and abiotic stress. In: Subramaniam G, Arumugam ., Rajendran, V (eds). Plant Growth Promoting Actinobacteria.Singapore: Springer, 2016, 203-12.

[150] Yandigeri MS, Meena KK, Singh D et al. Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul. 2012; 68: 411-20.

[151] Kurapova A, Zenova G, Sudnitsyn I et al. Thermotolerant and thermophilic actinomycetes from soils of Mongolia desert steppe zone. Microbiology. 2012; 81: 98-108.

[152] Abdallah M, Haroun S, Gomah A et al. Application of actinomycetes as biocontrol agents in the management of onion bacterial rot diseases. Arch Phytopathol Plant Prot. 2013; 46: 1797-808.

[153] Soltanzadeh M, Soltani Nejad M, Shahidi Bonjar GH . Application of soil-borne Actinomycetes for biological control against fusarium wilt of chickpea (Cicer arietinum) caused by Fusarium solani Fsp pisi. J Phytopathol. 2016; 164: 967-78.

[154] Bucher M, Hause B, Krajinski F et al. Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol. 2014; 204: 833-40.

[155] Luginbuehl LH, Menard GN, Kurup S et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science. 2017; 356: 1175-8.

[156] Bravo A, Brands M, Wewer V et al. Arbuscular mycorrhiza-specific enzymes FatM and RAM 2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol. 2017; 214: 1631-45.

[157] Balestrini R, Chitarra W, Fotopoulos V et al. Potential role of beneficial soil microorganisms in plant tolerance to abiotic stress factors. In: Lukac M, Grenni P, Gamboni M (eds). Soil Biological Communities and Ecosystem Resilience.Cham: Springer, 2017, 191-207.

[158] Jeong K, Mattes N, Catausan S et al. Genetic diversity for mycorrhizal symbiosis and phosphate transporters in rice. J Integr Plant Biol. 2015; 57: 969-79.

[159] Shi J, Zhao B, Zheng S et al. A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell. 2021; 184: 5527-5540.e18.

[160] Pozo MJ, Zabalgogeazcoa I, de Aldana BRV et al. Untapping the potential of plant mycobiomes for applications in agriculture. Curr Opin Plant Biol. 2021; 60: 102034.

[161] Ramírez-Flores MR, Perez-Limon S, Li M et al. The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation. elife. 2020; 9: e61701.

[162] Berger F, Gutjahr C . Factors affecting plant responsiveness to arbuscular mycorrhiza. Curr Opin Plant Biol. 2021; 59: 101994.

[163] Sawers RJ, Ramírez-Flores MR, Olalde-Portugal V et al. The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: insights from genetics and genomics. New Phytol. 2018; 220: 1135-40.

[164] Hetrick BAD, Wilson GWT, Cox TS . Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot. 1992; 70: 2032-40.

[165] Sawers RJ, Gutjahr C, Paszkowski U . Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci. 2008; 13: 93-7.

[166] Hohmann P, Messmer MM . Breeding for mycorrhizal symbiosis: focus on disease resistance. Euphytica. 2017; 213: 1-11.

[167] Zuccaro A, Langen G . Breeding for resistance: can we increase crop resistance to pathogens without compromising the ability to accommodate beneficial microbes? New Phytol. 2020; 227: 279-82.

[168] Lehnert H, Serfling A, Enders M et al. Genetics of mycorrhizal symbiosis in winter wheat (Triticum aestivum). New Phytol. 2017; 215: 779-91.

[169] Berruti A, Lumini E, Balestrini R et al. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol. 2016; 6: 1559.

[170] Rillig MC, Sosa-Hernández MA, Roy J et al. Towards an integrated mycorrhizal technology: harnessing mycorrhiza for sustainable intensification in agriculture. Front Plant Sci. 2016; 7: 1625.

[171] Rillig MC, Aguilar-Trigueros CA, Anderson IC et al. Myristate and the ecology of AM fungi: significance, opportunities, applications and challenges. New Phytol. 2020; 227: 1610-4.

[172] Sugiura Y, Akiyama R, Tanaka S et al. Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi. Proc Natl Acad Sci. 2020; 117: 25779-88.