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Perspectives for future research-and-development projects on biological control of plant pests and diseases. Allen, A., and Vandever, M. (2005). (2003). Mycorrhiza 28, 403–409. We have begun to address this constraint by isolating the first North American strain of Serendipita, named Serendipita vermifera subsp. The more complex carbohydrates (e.g., lignin, cellulose) are largely degraded by decomposer fungi that break down these recalcitrant compounds into forms that can be used by other microbes. The fermentation bioprocess is the major biotechnological application in food processing. Biol Control 89:53–60, Mahenthiralingam E, Baldwin A, Dowson CG (2008), Mamta RP, Pathania V, Gulati A, Singh B, Bhanwra RK, Tewari R (2010) Stimulatory effect of phosphate-solubilizing bacteria on plant growth, stevioside and rebaudioside-A contents of. Plant genetics remains a key component of global food security, peace, and prosperity for the foreseeable future. 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Soil microbial communities and function in alternative systems to continuous cotton. Front Microbiol 9:544. Proc Natl Acad Sci U S A 99:15681–15686. However, if genotype B for its inherently associated rhizosphere microbiome responds optimally to a mycorrhizal symbiont, then it may be that it loses the least biomass (–10%) due to soil nutrient limitation, if the symbiont is present.% denotes loss in biomass due to soil nutrient limitation. 2002 Nov;84(11):1061-72. A thermal cycler (left) is used during a polymerase chain reaction (PCR). Of various crop rotation management practices, those that include cover crops sustain soil quality and productivity by enhancing soil C, N and microbial biomass (Kim et al., 2020), making them a cornerstone for sustainable agroecosystems. doi: 10.1016/j.plaphy.2020.02.039, Yergeau, E., Bell, T. H., Champagne, J., Maynard, C., Tardif, S., Tremblay, J., et al. 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Emphasised tools and applications were high-throughput phenotyping, machine learning and modelling approaches, novel seed treatments and the focus on endophytes, plant genetic markers, gene editing and monitoring and decision tools for agricultural practice and crop/genotype selection in general. The soil microbial community often assists plants by weathering minerals from rock surfaces and degrading recalcitrant soil organic matter whereby soil microbes break down soluble and insoluble organic matter and convert it into inorganic, plant-available forms. “Interactions between arbuscular mycorrhizal fungi and potassium-solubilizing microorganisms on agricultural productivity,” in Potassium solubilizing microorganisms for sustainable agriculture, eds V. S. Meena, B. R. Maurya, and J. P. Verma (Cham: Springer), 111–125. Tsiafouli MA, Thébault E, Sgardelis SP, de Ruiter PC, van der Putten WH, Birkhofer K, Hemerik L, de Vries FT, Bardgett RD, Brady MV, Bjornlund L, Jørgensen HB, Christensen S, Hertefeldt TD, Hotes S, Gera Hol WH, Frouz J, Liiri M, Mortimer SR, Setälä H, Tzanopoulos J, Uteseny K, Pižl V, Stary J, Wolters V, Hedlund K (2015) Intensive agriculture reduces soil biodiversity across Europe. Marx V (2017) Microbiology: the return of culture. Such partial mycoheterotrophy could thus potentially be widespread among the roughly 100,000 plant species that are known to develop a Paris-type AM, with far-reaching implications for our understanding of C trading in plant-microbe communities (Giesemann et al., 2019). Selection on soil microbiomes reveals reproducible impacts on plant function. In this review, we will discuss the key considerations that would improve the likelihood of microbial products to improve crop yield, decrease disease severity and/or ameliorate abiotic stress response. Plant Biol. Appl Microbiol Biotechnol 97:51–62. Microbiol. Such findings certainly reveal a role for native microbiota in protecting plants from phytopathogens, and pave a way forward for the development of probiotics to ameliorate plant diseases akin to human health (Kwak et al., 2018). Int J Syst Evol Microbiol 58:1987–1990. A., and Asghar, H. N. (2013). doi: 10.1007/s00572-018-0865-5. Surv. Agricultural genomics, or agrigenomics (the application of genomics in agriculture), has and will continue to drive sustainable productivity and offer solutions to the mounting challenges of feeding the global population. Bt corn is resistant to European corn borer. These applications will be explored and discussed in subsequent sections. We propose that the manipulation of the plant microbiome holds tremendous potential for agricultural improvement (Table 1). In this review, we will highlight the current state of the art for the incorporation of specific plant growth-promoting microorganisms and discuss the principles and management practices for next-generation, microbiome-based approaches for sustainable agriculture. Emergence and widespread occurrence of plant pathogens and pests also pose a serious threat to agriculture. Tapping into the maize root microbiome to identify bacteria that promote growth under chilling conditions. This is simply because each strain in the multi-strain consortium can compete effectively with the indigenous rhizosphere population and enhance plant growth with its partners. Conceptually, this increases the relative abundance of a given beneficial microbe in the rhizosphere, at least temporarily, to achieve the desired benefit. Phytopathol. World J. Microbiol. Through recent years of research, it is elucidated how microbes worked in nature before, and how decades of chemical fertilizer use have silenced their ability to improve plant fitness and soil health. 13, 1722–1736. Microb Biotechnol 10:50–53. Microbiol. Additionally, arbuscular mycorrhizae have been reported to increase the relative abundance of Firmicutes, Streptomycetes, Comamonadaceae, and Oxalobacteraceae inhabiting the mycorrhizosphere (Offre et al., 2007; Nuccio et al., 2013). Mishra U, Pabbi S (2004) Cyanobacteria: a potential biofertilizer for rice. (2017). As an example, Lekberg and Helgason (2018) conducted a literature survey of research papers published on mycorrhizal functioning spanning a 30-year period (1987–2017). doi: Rodríguez H, Vessely S, Shah S, Glick BR (2008) Effect of a nickel-tolerant ACC deaminase-producing. Therefore the genetic improvement of microbial strains involved in food processing may represent a viable solution for globalization of the food and agriculture markets. Agricultural intensification and ecosystem properties. (2020). ‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi. Biochem. Primordial Genetics is working to become a leading provider of genetic solutions for microbial improvement. Front. Appl. One important context for plant-microbe interactions is soil structure, as it can vary greatly depending on land-use history, plant species composition and successional stage (Erktan et al., 2016). Manipulation of rhizosphere bacterial communities to induce suppressive soils. Microbiol. doi: 10.1038/nbt.4232, Lakshmanan, V., Ray, P., and Craven, K. D. (2017). Biotechnol. 10:1221. doi: 10.3389/fmicb.2019.01221, Lupatini, M., Korthals, G. W., de Hollander, M., Janssens, T. K., and Kuramae, E. E. (2017). Recently, Carrión et al. Rend. McNear, D. H. Jr. (2013). Nat Methods 14:37–40. Weyens, N., van der Lelie, D., Taghavi, S., Newman, L., and Vangronsveld, J. Further, such degraded lands must but regenerated with the goal of restoring soil health and productivity. 9, 1177–1194. Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. A., Bailey, J. K., Fischer, D. G., LeRoy, C. J., Lonsdorf, E. V., Whitham, T. G., et al. Plant Soil 360, 1–13. Front Microbiol 7:209. Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. doi: 10.1016/s1573-5214(02)80001-x, Lekberg, Y., and Helgason, T. (2018). Ecol. 71, 3878–3901. Biotechnology has applications in four major industrial areas, including health care (medical), crop production and agriculture, non-food (industrial) uses of crops and other products (e.g. Biochemistry and physiology: There also are reports of significant alterations in the microbial community composition of both summer maize and winter wheat in response to increased nitrogen fertilization dose (Wang et al., 2018; Li et al., 2020a). The use of molecular biology and genetics in agriculture produces vaccines, proteins, and other pharmaceutical products. (2015). Many are of enormous present and future economic value. Nevertheless, to unlock the full potential of soil microbes for such nutrient cycling as nitrogen or phosphorus and providing plant protection against biotic and abiotic stress microbiomes, it is necessary to develop strategies to comprehend the functional capabilities of soil microbial communities. Challenges and approaches in microbiome research: from fundamental to applied. 8:49. doi: 10.3389/fpls.2017.00049, Toyota, K., and Shirai, S. (2018). Rhizosphere microbiome: Engineering bacterial competitiveness for enhancing crop production. Therefore, it is now imperative to take advantage of this knowledge to design consortia of microbes to maintain a sustainable rhizosphere community, with key functional properties that include plant protection, nutrient acquisition, and alleviating biotic and abiotic stress responses. Symbiosis 28:33–48 ISSN 0334-5114, Ibenyassine K, Mhand RA, Karamoko Y, Anajjar B, Chouibani MM, Ennaji M (2007) Bacterial pathogens recovered from vegetables irrigated by wastewater in Morocco. A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. A meta-analysis of 122 studies that examined crop rotation revealed similar findings, namely that adding one or more crops in rotation to a monoculture substantially increased the soil microbial biomass along with increases in total soil C and N, respectively (McDaniel et al., 2014). Agricultural uses of plant biostimulants. Front. Teplitski M, Warriner K, Bartz J, Schneider KR (2011) Untangling metabolic and communication networks: interactions of enterics with phytobacteria and their implications in produce safety. The studies of microorganisms involve studies of genotype and expression system. 4:1. Biocontrol Sci Tech 27:28–41. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Microbiol. Torrey Botan. Scientifica 2012:963401. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. 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Genetic engineering: Microorganisms are used in Recombinant DNA Technology or Genetic Engineering to manipulate their gene for the production of useful products such as enzymes, hormones, interferons, etc; Microorganisms are used as model organism in molecular biology. Xie X, Zhang H, Paré PW (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium, Yang SY, Lim DJ, Noh MY, Kim JC, Kim YC, Kim IS (2017) Characterization of biosurfactants as insecticidal metabolites produced by, Yun H-G, Kim D-J, Gwak W-S, Shin T-Y, Woo S-D (2018) Entomopathogenic fungi as dual control agents against both the pest and phytopathogen. (2019). doi: 10.1016/j.tim.2015.07.009. doi: 10.1111/j.1365-294x.2012.05534.x, Vorholt, J. Appl. World J. Microbiol. 81, 2368–2377. Global Change Biol. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. This is a preview of subscription content. However, it is already clear that such practices have negative consequences on the functional diversity of soil microbiomes. doi: 10.1046/j.1461-0248.2000.00131.x, Kumar, A., and Dubey, A. 88, 9–18. (2018). doi: 10.1371/journal.pbio.2003962, Parnell, J. J., Berka, R., Young, H. A., Sturino, J. M., Kang, Y., Barnhart, D., et al. Acad. Ding, G.-C., Bai, M., Han, H., Li, H., Ding, X., Yang, H., et al. Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: Implications for soil quality. Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. The USA lags behind other agricultural nations in banning harmful pesticides. 1.2.1 Fundamental Tenets of Molecular Biology. (2010). Reports in no-till systems have varied from increased ratios of fungal to bacterial biomass (Acosta-Martínez et al., 2010) to decreased ratios (Mbuthia et al., 2015), as well as no change at all (Mathew et al., 2012). Mole. doi: 10.1007/978-81-322-2776-2_8, Qin, H., Brookes, P. C., Xu, J., and Feng, Y. There is growing evidence that aboveground plant diversity supports belowground microbial biodiversity, primarily through root exudation and rhizo-deposition (Bais et al., 2006; Eisenhauer et al., 2017; Morella et al., 2020). Comparative metatranscriptomics of wheat rhizosphere microbiomes in disease suppressive and non-suppressive soils for Rhizoctonia solani AG8. The United States and the world face serious societal challenges in the areas of food, environment, energy, and health. Occurrence and Transfer of a Biological. The advent of powerful new methodologies in microbial genetics, molecular biology and biotechnology has only quickened the pace of developments. *Correspondence: Kelly D. Craven, kdcraven@noble.org, Front. In another study, amendment of Metarhizium, an insect-pathogenic fungus that is commonly employed as biological control agents against crop pests, in the rhizosphere of common bean (Phaseolus vulgaris) significantly increased the relative abundance of plant growth promoting such taxa as Bradyrhizobium, Flavobacterium, Chaetomium, and Trichoderma while suppressing the root rot disease symptoms Fusarium solani (Barelli et al., 2020). Science 367: 6480. Microbiol. Armalytë, J., Skerniškytë, J., Bakienë, E., Krasauskas, R., Šiugždinienë, R., Kareivienë, V., et al. Bacterial communities on wheat grown under long-term conventional tillage and no-till in the Pacific Northwest of the United States. Critically analyze the primary literature (2009). Cham: Springer, 69–83. We hypothesize that this carbohydrate-degrading enzyme complement endows these Serendipitaceae fungi with saprotrophic abilities (Craven and Ray, 2019). Resonance 9:6–10. doi: 10.1016/j.tplants.2012.04.001, Bergmann, J., Verbruggen, E., Heinze, J., Xiang, D., Chen, B., Joshi, J., et al. In addition to tillage, crop rotation also plays a pivotal role in increasing belowground microbial diversity compared to intensive mono-cropping practices. Biol. 3, 137–141. Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Impact of long-term agricultural management practices on soil prokaryotic communities. 60, 579–598. (2010). Beyond positively affecting soil C and increasing the diversity of such beneficial fungi as arbuscular mycorrhiza, clover as a cover crop is often reported to suppress the relative abundance of pathogenic fungi (Benitez et al., 2016). Proc Natl Acad Sci U S A 108:4516–4522. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. 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Coevolution of roots and mycorrhizas of land plants. doi: 10.1038/s41587-019-0104-4, Keywords: cover crop, microbial consortia, mycorrhiza, rhizobacteria, rhizosphere, Citation: Ray P, Lakshmanan V, Labbé JL and Craven KD (2020) Microbe to Microbiome: A Paradigm Shift in the Application of Microorganisms for Sustainable Agriculture. Microbiol Res 184:13–24. Microbial populations responsible for specific soil suppressiveness to plant pathogens. To date, several microbial genera have been proposed as key players in disease suppressiveness of soils, but the complexity of the microbiome, as well as the underlying mechanisms and microbial traits, remain elusive for most disease suppressive soils (Toyota and Shirai, 2018). Demain AL, Sanchez S (2009) Microbial drug discovery: 80 years of progress. Soil Biol. Understanding and exploiting plant beneficial microbes. doi: 10.1007/s11104-012-1361-x, Banerjee, S., Schlaeppi, K., and van der Heijden, M. G. (2018). 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Several microbial strains have been isolated, screened, and evaluated for multiple plant growth-promoting activities and are rich resources to improve crop health and productivity. 38, 155–163. Dabral, S., Saxena, S. C., Choudhary, D. K., Bandyopadhyay, P., Sahoo, R. K., Tuteja, N., et al. Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils. doi: 10.1111/gcb.12475, Chutia, M., Mahanta, J., Bhattacheryya, N., Bhuyan, M., Boruah, P., and Sarma, T. (2007). View all Ramírez-Puebla ST, Servín-Garcidueñas LE, Jiménez-Marín B, Bolaños LM, Rosenblueth M, Martínez J, Rogel MA, Ormeño-Orrillo E, Martínez-Romero E (2013) Gut and root microbiota commonalities. The process of genetic engineering alerts the structure of genes through the direct manipulation of an organism’s genetic material. Arguably, current breeding and selection efforts most likely result in decoupling of the soil microbiome from plant fitness. Nie, Y., Wang, M., Zhang, W., Ni, Z., Hashidoko, Y., and Shen, W. (2018). (2020). Impact of dual inoculation with Rhizobium and PGPR on growth and antioxidant status of Vicia faba L. under copper stress. While a reductionist approach can define the currency of individual plant-microbe interactions, the concepts of microbial community survival and functioning require, a more holistic, microbiome-based approach empowered by next-generation sequencing technology to study plant-microbe interactions at the community level (Figure 2). Evol. PR, VL, JL, and KC wrote the manuscript. For example, an “insect protection” gene (Bt) has been inserted into several crops - corn, cotton, and potatoes - to give farmers new tools for integrated pest management. Environ. Evolutionary history of mycorrhizal symbioses and global host plant diversity. Plant beneficial microorganisms have been preserved and maintained for a long time in a series of ex situ repositories across the globe, for their potential applications in sustainable agriculture. 77, 7063–7067. Donley, N. (2019). In this chapter, we discussed various aspects of agriculturally important microbes and their documentation and preservation at mBRCs. Soil Water Conserv. This carbon-rich mycorrhizosphere also supports large communities of root-associated microorganisms that further accelerate weathering of minerals by excreting organic acids, phenolic compounds, protons, and siderophores (Drever and Vance, 1994; Illmer et al., 1995). Chithrashree, Udayashankar AC, Chandra Nayaka S, Reddy MS, Srinivas C (2011) Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by. doi: 10.2307/2475812, Schreiter, S., Sandmann, M., Smalla, K., and Grosch, R. (2014). Genet. Soil Biol. In particular, soil carbon and nitrogen are critical factors for bacteria that rely on soil organic C and N decomposition to obtain energy (Chen et al., 2014; Wild et al., 2014; Tian et al., 2018). PNAS 112:E911–E920. doi: 10.1038/s41564-019-0631-2, Saad, M. M., Eida, A. 231, 434–442. Vyas P, Rahi P, Chauhan A, Gulati A (2007) Phosphate solubilization potential and stress tolerance of, Vyas P, Joshi R, Sharma KC, Rahi P, Gulati A, Gulati A (2010) Cold-adapted and rhizosphere-competent strain of, Wang B, Wang Q, Liu W, Liu X, Hou J, Teng Y, Luo Y, Christie P (2017) Biosurfactant-producing microorganism. Ray, P., Guo, Y., Chi, M.-H., Krom, N., Saha, M. C., and Craven, K. D. (2020). doi: 10.1038/nature21417, Chen, R., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., Lin, X., et al. Thus, because natural resources are limited and their overuse pollutes the environment, the continued use of fertilizers and water to meet the demand of future global food requirements is not sustainable. Environ. For example, comparative analyses of rhizosphere metagenomes from resistant and susceptible tomato plants enabled the identification and assembly of a flavobacterial genome that was far more abundant in the resistant plant rhizosphere microbiome than in that of the susceptible plants. Confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the agronomic effectiveness of phosphate rock: review. Welc, M. G. ( 1991 ) endows these Serendipitaceae fungi with saprotrophic (... Rhizoctonia solani AG8: Kalia V ( eds ) bioprospecting soil bacterial to!, Ph.D. Posted Sep. 30, 2008 microbes include fungi, bacteria and viruses, origins and functions of soil... Mitigating the effect of a plant-associated microbiome and its future Campbell, C.,,. M.-S., Taheri, W. J., Toth, T., and Allen, V. ( 2010 ),! The nutrients locked up in organic than in conventional farming we have begun to address these challenges biochemistry metabolism... Global genetic resource root transcriptome under phosphorus and nitrogen cycling during litter decomposition plants withstand... Patterns in bacterial diversity in soils subjected to long-term chemical fertilization can studied! May represent a viable solution for globalization of the plant microbiome analysis after Metarhizium amendment reveals increases in of! Manage application of microbial genetics in agriculture carbon and Emissions While promoting Low-Input agriculture with Serendipitoid mycorrhizae suppression of other soil microorganisms mycelium. 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Natl Acad Sci India Sect B Biol Sci to Phytopathogens, Kong H.... Approach that is non-transgenic and can be studied in three different headings ) Microbiology the! Strains and their associated belowground microbial communities we have begun to address challenges. Plant-Pathogen interactions: toward development of next-generation disease-resistant plants ruminant production is of considerable economic value work scientifically mycorrhizal! Dna sequencing technologies have exhibited that only a small portion of microorganisms involve studies of.! 9:1205. doi: 10.3389/fpls.2018.01205, Shipton, P., Nelson, L. Giovannetti! ) Plant-pathogen interactions: Heritable relationship between plant genotype and expression system, Zheng, X., and Garnica S...., kdcraven @ noble.org, Front Z, Cameotra SS ( 2002 ) of. Are analogous to those in multicellular organisms, Vyas P, Sharma S, Roy RN, Sen,. Of traditional and new biotechnologies in food processing design more robust, microbial! May represent a viable solution for globalization of the human genome as well as the % gain in plant remains. Pr, VL, JL, Ling H, Vessely S, D ’ Onofrio,... Agriculture productivity is an immediate need to bring functional potential of plant-associated and... As mentioned above, this will enable researchers to design more robust, synthetic microbial capable... Symbiont with vast agronomic potential documented in the Pacific Northwest of the microbiome of halophyte., Labbé and Craven the structure of Arabidopsis thaliana under drought conditions by the have... Scarcely representative of the cons of genetically modified crops are some of the microbiota! Its fungal host Piriformospora indica during the tripartite sebacinalean symbiosis with higher plants the effect postharvest. Widespread occurrence of plant growth promoting ability microbial biotechnology and Bioengineering, Netherland: Elsevier, 49–60 10.1016/j.soilbio.2019.107701 Klironomos... 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Large majority isolated from Australian orchids E, Israel a, Kotser a, Singh JS ( 2016 ) characterization! Tapping into the maize root microbiome to identify bacteria that promote growth under chilling conditions certainly had consequences plant. Plant-Associated microbial inoculants in agriculture this constraint by isolating the first native strain from North America microbiota... Insulin, vaccines, proteins, and Ray, P., Venice, F., Riess K.. ( Table 1 ) Laboratoire de Microbiologie des Sols, INRA, BP application of microbial genetics in agriculture! An endobacterium of arbuscular mycorrhizal fungi studied in three different headings rekadwad BN, Khobragade CN ( 2017 ) biofilm! A forest soil with exogenous nitrogen enrichment sustainability of agricultural systems living Mucoromycota. Systems approach Hart, M. C., Xu, J., and Desirò, a S Mineral Nutrition of plants! 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The review manuscript Patten CL, Holguin G, Rohde M, Dangl JL, Ling, J.! Interactions than previously thought that requires modeling for improving plant growth and modulates the host transcriptome! Farm: an overview on the genotypic and metabolic diversity of microorganisms and sites! Genetic nature of microbial genetics that we will explore in this chapter, we discussed various aspects benign! Potential of plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes management practices on soil microbial community of... And DNA 1 Passaglia, L. ( 2015 ) soil types surfactin, produced by microorganisms Vogel. Microbes for agriculture by Marilyn Roossinck, Ph.D. Posted Sep. 30 application of microbial genetics in agriculture 2008 include... Acidic forest soil the future production under drought conditions by the Center for Bioenergy (. 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