Plant-Microbe Interactions - Insights and Views for Applications in Sustainable Agriculture

Anne Sahithi Somavarapu Thomas, Wasinee Pongprayoon, Kraipat Cheenkachorn, Malinee Sriariyanun

Abstract

The term “microbiome” refers to the association of plants with various microorganisms which play an important role in the niches they occupy. These microorganisms are found in the endosphere, phyllosphere, and rhizosphere, of host plants which are involved in plant ecology and physiology. The structure and dynamics of the plant microbiome have been significant seen in the last few years. In addition, the plant microbiome enhances the host plant with gene pools, which is referred to as the second plant genome or extended genome. Interestingly, the microbiome associated with plant roots has received unique attention in recent years due to its important role in host nutrition, immunity, and development. Prospective studies of the microbiome have been coupled with the need for more sustainable production for agriculture. On the other hand, various environmental factors are associated with plant-microbiome interactions that can affect composition and diversity. This review provides insights and views of plant microbiome for sustainable agriculture. Host factors that influence the microbial community, root-associated microbial consortium, commercial application, and limitation of plant microbiome were discussed. Also, this review provides current knowledge of the plant microbiome into potential biotechnology products that can be used in agricultural systems. Regardless, microbiome innovation represents the future of sustainable agriculture.

Keywords

References

[1] G. Berg, D. Rybakova, M. Grube, and M. Köberl, “The plant microbiome explored: Implications for experimental botany,” Journal of Experimental Botany, vol. 67, no. 4, pp. 995–1002, Feb. 2016.

[2] M. McFall-Ngai, M. G. Hadfield, T. C. G. Bosch, H. V. Carey, T. Do.-Lošo, A. E. Douglas, N. Dubilier, G. Eberl, T. Fukami, S. F. Gilbert, U. Hentschel, N. King, S. Kjelleberg, A. H. Knoll, N. Kremer, S. K. Mazmanian, J. L. Metcalf, K. Nealson, N. E. Pierce, J. F. Rawls, A. Reid, E. G. Ruby, M. Rumpho, J. G. Sanders, D. Tautz, and J. J. Wernegreen, “Animals in a bacterial world, a new imperative for the life sciences,” Proceedings of the National Academy of Sciences, vol. 110, no. 9, pp. 3229– 3236, Feb. 2013.
[3] D. Bulgarelli, M. Rott, K. Schlaeppi, E. V. L. van Themaat, N. Ahmadinejad, F. Assenza, P. Rauf, B. Huettel, R. Reinhardt, E. Schmelzer, J. Peplies, F. O. Gloeckner, R. Amann, T. Eickhorst, and P. Schulze-Lefert, “Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota,” Nature, vol. 488, no. 7409, pp. 91–95, Aug. 2012.

[4] R. L. Berendsen, C. M. J. Pieterse, and P. A. H. M. Bakker, “The rhizosphere microbiome and plant health,” Trends in Plant Science, vol. 17, no. 8, pp. 478–486, Aug. 2012.

[5] I. Zilber-Rosenberg and E. Rosenberg, “Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution,” FEMS Microbiology Reviews, vol. 32, no. 5, pp. 723–735, Aug. 2008.

[6] R. T. Koide and B. Mosse, “A history of research on arbuscular mycorrhiza,” Mycorrhiza, vol. 14, no. 3, pp. 145–163, Jun. 2004.

[7] D. S. Heckman, “Molecular evidence for the early colonization of land by fungi and plants,” Science, vol. 293, no. 5532, pp. 1129–1133, Aug. 2001.

[8] D. Bulgarelli, K. Schlaeppi, S. Spaepen, E. V. L. van Themaat, and P. Schulze-Lefert, “Structure and functions of the bacterial microbiota of plants,” Annual Review of Plant Biology, vol. 64, no. 1, pp. 807–838, Apr. 2013.

[9] S. Thijs, W. Sillen, F. Rineau, N. Weyens, and J. Vangronsveld, “Towards an enhanced understanding of plant–microbiome interactions to improve phytoremediation: Engineering the metaorganism,” Frontiers in Microbiology, vol. 7, p. Mar. 2016.

[10] K. M. G. Dastogeer, H. Li, K. Sivasithamparam, M. G. K. Jones, and S. J. Wylie, “Host specificity of endophytic mycobiota of wild nicotiana plants from Arid Regions of Northern Australia,” Microbial Ecology, vol. 75, no. 1, pp. 74–87, Jan. 2018.

[11] K. M. G. Dastogeer, H. Li, K. Sivasithamparam, M. G. K. Jones, and S. J. Wylie, “Fungal endophytes and a virus confer drought tolerance to Nicotiana benthamiana plants through modulating osmolytes, antioxidant enzymes and expression of host drought responsive genes,” Environmental and Experimental Botany, vol. 149, pp. 95–108, May 2018.

[12] K. Schlaeppi, N. Dombrowski, R. G. Oter, E. V. L. van Themaat, and P. Schulze-Lefert, “Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives,” Proceedings of the National Academy of Sciences, vol. 111, no. 2, pp. 585–592, Jan. 2014.

[13] K. M. G. Dastogeer, H. Li, K. Sivasithamparam, M. G. K. Jones, X. Du, Y. Ren, and S. J. Wylie, “Metabolic responses of endophytic Nicotiana benthamiana plants experiencing water stress,” Environmental and Experimental Botany, vol. 143, pp. 59–71, Nov. 2017.

[14] P. Hinsinger, A. G. Bengough, D. Vetterlein, and I. M. Young, “Rhizosphere: Biophysics, biogeochemistry and ecological relevance,” Plant and Soil, vol. 321, no. 1–2, pp. 117–152, Aug. 2009.

[15] M. Bonkowski, C. Villenave, and B. Griffiths, “Rhizosphere fauna: The functional and structural diversity of intimate interactions of soil fauna with plant roots,” Plant and Soil, vol. 321, no. 1–2, pp. 213–233, Aug. 2009.

[16] Ö. İnceoğlu, W. A. Al-Soud, J. F. Salles, A. V. Semenov, and J. D. van Elsas, “Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing,” PLoS ONE, vol. 6, no. 8, p. e23321, Aug. 2011.

[17] J. Gans, “Computational improvements reveal great bacterial diversity and high metal toxicity in soil,” Science, vol. 309, no. 5739, pp. 1387–1390, Aug. 2005.
[18] M. G. A. Heijden, F. M. Martin, M. Selosse, and I. R. Sanders, “Mycorrhizal ecology and evolution: The past, the present, and the future,” New Phytologist, vol. 205, no. 4, pp. 1406–1423, Mar. 2015.

[19] E. H. Lee, J. K. Eo, K. H. Ka, and A. H. Eom, “Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems,” Mycobiology, vol. 41, no. 3, pp. 121–125, Sep. 2013.

[20] O. M. Finkel, A. Y. Burch, S. E. Lindow, A. F. Post, and S. Belkin, “Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree,” Applied and Environmental Microbiology, vol. 77, no. 21, pp. 7647–7655, Nov. 2011.

[21] J. A. Vorholt, “Microbial life in the phyllosphere,” Nature Reviews Microbiology, vol. 10, no. 12, pp. 828–840, Dec. 2012.

[22] S. E. Lindow and M. T. Brandl, “Microbiology of the phyllosphere,” Applied and Environmental Microbiology, vol. 69, no. 4, pp. 1875–1883, Apr. 2003.

[23] M. Grover, S. Z. Ali, V. Sandhya, A. Rasul, and B. Venkateswarlu, “Role of microorganisms in adaptation of agriculture crops to abiotic stresses,” World Journal of Microbiology and Biotechnology, vol. 27, no. 5, pp. 1231–1240, May 2011.

[24] F. D. Andreote, T. Gumiere, and A. Durrer, “Exploring interactions of plant microbiomes,” Scientia Agricola, vol. 71, no. 6, pp. 528–539, Dec. 2014.

[25] J. Liu, Z. Meng, X. Liu, and X.-H. Zhang, “Microbial assembly, interaction, functioning, activity and diversification: a review derived from community compositional data,” Marine Life Science & Technology, vol. 1, no. 1, pp. 112–128, Nov. 2019.
[26] G. Berg, M. Grube, M. Schloter, and K. Smalla, “Unraveling the plant microbiome: Looking back and future perspectives,” Frontiers in Microbiology, vol. 5, p. Jun. 2014.

[27] F. D. Andreote, U. N. da Rocha, W. L. Araújo, J. L. Azevedo, and L. S. van Overbeek, “Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum),” Antonie van Leeuwenhoek, vol. 97, no. 4, pp. 389–399, May 2010.

[28] P. A. Rodriguez, M. Rothballer, S. P. Chowdhury, T. Nussbaumer, C. Gutjahr, and P. Falter-Braun, “Systems biology of plant-microbiome interactions,” Molecular Plant, vol. 12, no. 6, pp. 804–821, Jun. 2019.

[29] J. Barea, J. Kotila, and F. Iachello, “0nββ and 2nββ nuclear matrix elements in the interacting boson model with isospin restoration,” Physical Review C - Nuclear Physics, vol. 91, no. 3, p. 2015.

[30] P. Trivedi, J. E. Leach, S. G. Tringe, T. Sa, and B. K. Singh, “Plant–microbiome interactions: From community assembly to plant health,” Nature Reviews Microbiology, vol. 18, no. 11, pp. 607–621, Nov. 2020.
[31] D. J. Baumgardner, “Soil-related bacterial and fungal infections,” The Journal of the American Board of Family Medicine, vol. 25, no. 5, pp. 734–744, Sep. 2012.

[32] O. S. Olanrewaju, A. S. Ayangbenro, B. R. Glick, and O. O. Babalola, “Plant health: Feedback effect of root exudates-rhizobiome interactions,” Applied Microbiology and Biotechnology, vol. 103, no. 3, pp. 1155–1166, Feb. 2019.

[33] J. Li, X. Lin, A. Chen, T. Peterson, K. Ma, M. Bertzky, P. Ciais, V. Kapos, C. Peng, and B. Poulter, “Global priority conservation areas in the face of 21st century climate change,” PLoS ONE, vol. 8, no. 1, p. e54839, Jan. 2013.

[34] N. Suzuki, R. M. Rivero, V. Shulaev, E. Blumwald, and R. Mittler, “Abiotic and biotic stress combinations,” New Phytologist, vol. 203, no. 1, pp. 32–43, Jul. 2014.

[35] C. Lesk, P. Rowhani, and N. Ramankutty, “Influence of extreme weather disasters on global crop production,” Nature, vol. 529, no. 7584, pp. 84–87, Jan. 2016.

[36] T. Ma and C. Zhou, “Climate-associated changes in spring plant phenology in China,” International Journal of Biometeorology, vol. 56, no. 2, pp. 269–275, Mar. 2012.

[37] J. Xia and S. Wan, “Independent effects of warming and nitrogen addition on plant phenology in the Inner Mongolian steppe,” Annals of Botany, vol. 111, no. 6, pp. 1207–1217, Jun. 2013.

[38] A. Majeed, M. K. Abbasi, S. Hameed, A. Imran, and N. Rahim, “Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion,” Frontiers in Microbiology, vol. 6, p. Mar. 2015.

[39] Y. N. Ho, H. M. Chiang, C. P. Chao, C. C, Su, H. F. Hsu, C. T. Guo, J. L. Hsieh, and C. C. Huang, “In planta biocontrol of soilborne Fusarium wilt of banana through a plant endophytic bacterium, Burkholderia cenocepacia 869T2,” Plant and Soil, vol. 387, no. 1–2, pp. 295–306, Feb. 2015.

[40] A. A. Navarrete, F. S. Cannavan, R. G. Taketani, and S. M. Tsai, “A molecular survey of the diversity of microbial communities in different amazonian agricultural model systems,” Diversity, vol. 2, no. 5, pp. 787–809, May 2010.

[41] F. Colombo, C. A. Macdonald, T. C. Jeffries, J. R. Powell, and B. K. Singh, “Impact of forest management practices on soil bacterial diversity and consequences for soil processes,” Soil Biology and Biochemistry, vol. 94, pp. 200–210, Mar. 2016.

[42] J. Estendorfer, B. Stempfhuber, P. Haury, G. Vestergaard, M. C. Rillig, J. Joshi, P. Schröder, and M. Schloter, “The influence of land use intensity on the plant-associated microbiome of Dactylis glomerata L.,” Frontiers in Plant Science, vol. 8, p. Jun. 2017.
[43] N. R. Gottel, H. F. Castro, M. Kerley, Z. Yang, D. A. Pelletier, M. Podar, T. Karpinets, E. Uberbacher, G. A. Tuskan, R. Vilgalys, M. J. Doktycz, and C. W. Schadt, “Distinct microbial communities within the endosphere and rhizosphere of populus deltoides roots across contrasting soil types,” Applied and Environmental Microbiology, vol. 77, no. 17, pp. 5934–5944, Sep. 2011.

[44] A. K. A. Suleiman, V. S. Pylro, and L. F. W. Roesch, “Replacement of native vegetation alters the soil microbial structure in the Pampa biome,” Scientia Agricola, vol. 74, no. 1, pp. 77–84, Feb. 2017.

[45] K. Jangid, M. A. Williams, A. J. Franzluebbers, T. M. Schmidt, D. C. Coleman, and W. B. Whitman, “Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties,” Soil Biology and Biochemistry, vol. 43, no. 10, pp. 2184–2193, Oct. 2011.

[46] G. Curlango-Rivera, D. A. Huskey, A. Mostafa, J. O. Kessler, Z. Xiong, and M. C. Hawes, “Intraspecies variation in cotton border cell production: Rhizosphere microbiome implications,” American Journal of Botany, vol. 100, no. 9, pp. 1706–1712, Sep. 2013.
[47] N. Bodenhausen, M. B.-Miller, M. Ackermann, and J. A. Vorholt, “A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota,” PLoS Genetics, vol. 10, no. 4, p. e1004283, Apr. 2014.

[48] M.-J. Kwak, H. G. Kong, K. Choi, S. K. Kwon, J. Y. Song, J. Lee, P. A. Lee, S. Y. Choi, M. Seo, H. J. Lee, E. J. Jung, H. Park, N. Roy, H. Kim, M. Min Lee, E. M. Rubin, S. W. Lee, and J. F. Kim, “Rhizosphere microbiome structure alters to enable wilt resistance in tomato,” Nature Biotechnology, vol. 36, no. 11, pp. 1100–1109, Nov. 2018.

[49] P. Ardanov, S. Lyastchenko, K. Karppinen, H. Häggman, N. Kozyrovska, and A. M. Pirttilä, “Effects of Methylobacterium sp. on emergence, yield, and disease prevalence in three cultivars of potato (Solanum tuberosum L.) were associated with the shift in endophytic microbial community,” Plant and Soil, vol. 405, no. 1–2, pp. 299–310, Aug. 2016.

[50] B. Mitter, N. Pfaffenbichler, R. Flavell, S. Compant, L. Antonielli, A. Petric, T. Berninger, M. Naveed, R. S.-Tezerji, G. von Maltzahn, and A. Sessitsch, “A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds,” Frontiers in Microbiology, vol. 8, p. Jan. 2017.

[51] L. Barelli, A. S. Waller, S. W. Behie, and M. J. Bidochka, “Plant microbiome analysis after Metarhizium amendment reveals increases in abundance of plant growth-promoting organisms and maintenance of disease-suppressive soil,” PLOS ONE, vol. 15, no. 4, p. e0231150, Apr. 2020.

[52] L. da Silva Lima, F. L. Olivares, R. Rodrigues de Oliveira, M. R. G. Vega, N. O. Aguiar, and L. P. Canellas, “Root exudate profiling of maize seedlings inoculated with Herbaspirillum seropedicae and humic acids,” Chemical and Biological Technologies in Agriculture, vol. 1, no. 1, p. 23, Dec. 2014.

[53] M. T. Agler, J. Ruhe, S. Kroll, C. Morhenn, S.-Tae Kim, D. Weigel, and E. M. Kemen, “Microbial hub taxa link host and abiotic factors to plant microbiome variation,” PLOS Biology, vol. 14, no. 1, p. e1002352, Jan. 2016.

[54] A. Erlacher, M. Cardinale, R. Grosch, M. Grube, and G. Berg, “The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome,” Frontiers in Microbiology, vol. 5, p. Apr. 2014.

[55] M. Köberl, M. Dita, A. Martinuz, C. Staver, and G. Berg, “Members of Gammaproteobacteria as indicator species of healthy banana plants on Fusarium wilt-infested fields in Central America,” Scientific Reports, vol. 7, no. 1, p. 45318, May 2017.

[56] W. Purahong, L. Orrù, I. Donati, G. Perpetuini, A. Cellini, A. Lamontanara, V. Michelotti, G. Tacconi, and F. Spinelli, “Plant microbiome and its link to plant health: Host species, organs and Pseudomonas syringae pv. actinidiae infection shaping bacterial phyllosphere communities of Kiwifruit plants,” Frontiers in Plant Science, vol. 9, p. Nov. 2018.

[57] V. M. Bergottini, V. Hervé, D. A. Sosa, M. B. Otegui, P. D. Zapata, and P. Junier, “Exploring the diversity of the root-associated microbiome of Ilex paraguariensis St. Hil. (Yerba Mate),” Applied Soil Ecology, vol. 109, pp. 23–31, Jan. 2017.

[58] M. Hartmann, B. Frey, J. Mayer, P. Mäder, and F. Widmer, “Distinct soil microbial diversity under long-term organic and conventional farming,” The ISME Journal, vol. 9, no. 5, pp. 1177–1194, May 2015.

[59] Z. Li, C. Zu, C. Wang, J. Yang, H. Yu, and H. Wu, “Different responses of rhizosphere and non-rhizosphere soil microbial communities to consecutive Piper nigrum L. monoculture,” Scientific Reports, vol. 6, no. 1, p. 35825, Dec. 2016.

[60] M. Simonin, C. Dasilva, V. Terzi, E. L. M. Ngonkeu, D. Diouf, A. Kane, G. Béna, and L. Moulin, “Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils,” FEMS Microbiology Ecology, vol. 96, no. 6, p. Jun. 2020.

[61] C. Santos-Medellín, J. Edwards, Z. Liechty, B. Nguyen, and V. Sundaresan, “Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes,” mBio, vol. 8, no. 4, p. Sep. 2017.

[62] C. R. Fitzpatrick, J. Copeland, P. W. Wang, D. S. Guttman, P. M. Kotanen, and M. T. J. Johnson, “Assembly and ecological function of the root microbiome across angiosperm plant species,” Proceedings of the National Academy of Sciences, vol. 115, no. 6, pp. E1157–E1165, Feb. 2018.

[63] M. van der Voort, M. Kempenaar, M. van Driel, J. M. Raaijmakers, and R. Mendes, “Impact of soil heat on reassembly of bacterial communities in the rhizosphere microbiome and plant disease suppression,” Ecology Letters, vol. 19, no. 4, pp. 375–382, Apr. 2016.

[64] A. Mark Ibekwe, S. Ors, J. F. S. Ferreira, X. Liu, and D. L. Suarez, “Seasonal induced changes in spinach rhizosphere microbial community structure with varying salinity and drought,” Science of The Total Environment, vol. 579, pp. 1485–1495, Feb. 2017.

[65] P. Vandenkoornhuyse, A. Quaiser, M. Duhamel, A. Le Van, and A. Dufresne, “The importance of the microbiome of the plant holobiont,” New Phytologist, vol. 206, no. 4, pp. 1196–1206, Jun. 2015.

[66] D. Kour, K. L. Rana, N. Yadav, A. N. Yadav, A. Kumar, V. S. Meena, B. Singh, V. S. Chauhan, H. S. Dhaliwal, and A. K. Saxena, “Rhizospheric microbiomes: Biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture,” in Plant Growth Promoting Rhizobacteria for Agricultural Sustainability. Singapore: Springer, 2019, pp. 19–65.

[67] N. N. AL-Jabri and M. A. Hossain, “Comparative chemical composition and antimicrobial activity study of essential oils from two imported lemon fruits samples against pathogenic bacteria,” Beni- Suef University Journal of Basic and Applied Sciences, vol. 3, no. 4, pp. 247–253, Dec. 2014.

[68] B. Orman-Ligeza, B. Parizot, P. P. Gantet, T. Beeckman, M. J. Bennett, and X. Draye, “Postembryonic root organogenesis in cereals: Branching out from model plants,” Trends in Plant Science, vol. 18, no. 8, pp. 459–467, Aug. 2013.

[69] B. Scheres, P. Benfey, and L. Dolan, “Root development,” The Arabidopsis Book, vol. 1, p. e0101, Jan. 2002.

[70] H. A. Contreras-Cornejo, L. Macías-Rodríguez, C. Cortés-Penagos, and J. López-Bucio, “Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in arabidopsis,” Plant Physiology, vol. 149, no. 3, pp. 1579–1592, Mar. 2009.
[71] S. Steinkellner, R. Mammerler, and H. Vierheilig, “Microconidia germination of the tomato pathogen Fusarium oxysporum in the presence of root exudates,” Journal of Plant Interactions, vol. 1, no. 1, pp. 23–30, Mar. 2005.

[72] S. Steinkellner and R. Mammerler, “Effect of flavonoids on the development of Fusarium oxysporum f. sp. lycopersici,” Journal of Plant Interactions, vol. 2, no. 1, pp. 17–23, Mar. 2007.

[73] S. Dong, Z. Tian, P. J. Chen, R. S. Kumar, C. H. Shen, D. Cai, R. Oelmüllar, and K. Wun Yeh, “The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots,” Journal of Experimental Botany, vol. 64, no. 14, pp. 4529–4540, Nov. 2013.

[74] S. von Felten, P. A. Niklaus, M. Scherer-Lorenzen, A. Hector, and N. Buchmann, “Do grassland plant communities profit from N partitioning by soil depth?,” Ecology, vol. 93, no. 11, pp. 2386–2396, Nov. 2012.

[75] A. Martínez-Medina, M. Del Mar Alguacil, J. A. Pascual, and S. C. M. Van Wees, “Phytohormone profiles induced by trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants,” Journal of Chemical Ecology, vol. 40, no. 7, pp. 804–815, Jul. 2014.

[76] A. Sofo, A. Scopa, M. Manfra, M. D. Nisco, G. Tenore, J. Troisi, R. D. Fiori, and E. Novellino, “Trichoderma harzianum strain T-22 induces changes in phytohormone levels in cherry rootstocks (Prunus cerasus × P. canescens),” Plant Growth Regulation, vol. 65, no. 2, pp. 421–425, Nov. 2011.

[77] R. Aloni, E. Aloni, M. Langhans, and C. I. Ullrich, “Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism,” Annals of Botany, vol. 97, no. 5, pp. 883–893, May 2006.

[78] D. P. Lohar, J. E. Schaff, J. G. Laskey, J. J. Kieber, K. D. Bilyeu, and D. M. Bird, “Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses,” The Plant Journal, vol. 38, no. 2, pp. 203–214, Apr. 2004.

[79] S. Chen, T. R. Waghmode, R. Sun, E. E. Kuramae, C. Hu, and B. Liu, “Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization,” Microbiome, vol. 7, no. 1, p. 136, Dec. 2019.

[80] L. Yang, J. Danzberger, A. Schöler, P. Schröder, M. Schloter, and V. Radl, “Dominant groups of potentially active bacteria shared by barley seeds become less abundant in root associated microbiome,” Frontiers in Plant Science, vol. 8, pp. 1–12, Jun. 2017.

[81] A. Mardanova, M. Lutfullin, G. Hadieva, Y. Akosah, D. Pudova, D. Kabanov, E. Shagimardanova, P. Vankov, S. Vologin, N. Gogoleva, Z. Stasevski, and M. Sharipova, “Structure and variation of root-associated microbiomes of potato grown in alfisol,” World Journal of Microbiology and Biotechnology, vol. 35, no. 12, p. 181, Dec. 2019.

[82] Y. Bashan, L. E. De-Bashan, S. R. Prabhu, and J.-P. Hernandez, “Advances in plant growth-promoting bacterial inoculant technology: Formulations and practical perspectives (1998–2013),” Plant and Soil, vol. 378, no. 1–2, pp. 1–33, May 2014.

[83] H. Chauhan and D. J. Bagyaraj, “Inoculation with selected microbial consortia not only enhances growth and yield of French bean but also reduces fertilizer application under field condition,” Scientia Horticulturae, vol. 197, pp. 441–446, Dec. 2015.

[84] N. K. Arora, T. Fatima, I. Mishra, and S. Verma, “Microbe-based inoculants: role in next green revolution,” in Environmental Concerns and Sustainable Development. Singapore: Springer, 2020, pp. 191–246.
[85] R. E. Karamanos, N. A. Flore, and J. T. Harapiak, “Re-visiting use of Penicillium bilaii with phosphorus fertilization of hard red spring wheat,” Canadian Journal of Plant Science, vol. 90, no. 3, pp. 265–277, May 2010.

[86] E. K. Mitter, M. Tosi, D. Obregón, K. E. Dunfield, and J. J. Germida, “Rethinking crop nutrition in times of modern microbiology: Innovative biofertilizer technologies,” Frontiers in Sustainable Food Systems, vol. 5, p. Feb. 2021.

[87] D. Ronga, F. Caradonia, L. Setti, D. Hagassou, C. V. Giaretta Azevedo, J. Milc, S. Pedrazzi, G. Allesina, L. Arru, and E. Francia, “Effects of innovative biofertilizers on yield of processing tomato cultivated in organic cropping systems in northern Italy,” Acta Horticulturae, no. 1233, pp. 129–136, Feb. 2019.

[88] P. Calvo, L. Nelson, and J. W. Kloepper, “Agricultural uses of plant biostimulants,” Plant and Soil, vol. 383, no. 1–2, pp. 3–41, Oct. 2014.

[89] M. Regvar, K. Vogel, N. Irgel, T. Wraber, U. Hildebrandt, P. Wilde, and H. Bothe, “Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi,” Journal of Plant Physiology, vol. 160, no. 6, pp. 615–626, Jan. 2003.

[90] J. Ramirez-Villegas, M. Salazar, A. Jarvis, and C. E. Navarro-Racines, “A way forward on adaptation to climate change in Colombian agriculture: Perspectives towards 2050,” Climatic Change, vol. 115, no. 3–4, pp. 611–628, Dec. 2012.

[91] K. Vishwakarma, N. Kumar, C. Shandilya, S. Mohapatra, S. Bhayana, and A. Varma, “Revisiting plant–microbe interactions and microbial consortia application for enhancing sustainable agriculture: A review,” Frontiers in Microbiology, vol. 11, p. Dec. 2020.

[92] E. T. Alori and O. O. Babalola, “Microbial inoculants for improving crop quality and human health in Africa,” Frontiers in Microbiology, vol. 9, Sep. 2018, doi: 10.3389/fmicb.2020.560406.

[93] C. L. Wilson and M. E. Wisniewski, “Biological control of postharvest diseases of fruits and vegetables: An emerging technology,” Annual Review of Phytopathology, vol. 27, no. 1, pp. 425– 441, Sep. 1989.

[94] K. Jawed, S. S. Yazdani, and M. A. Koffas, “Advances in the development and application of microbial consortia for metabolic engineering,” Metabolic Engineering Communications, vol. 9, p. e00095, Dec. 2019.

[95] M. O’Callaghan, “Microbial inoculation of seed for improved crop performance: Issues and opportunities,” Applied Microbiology and Biotechnology, vol. 100, no. 13, pp. 5729–5746, Jul. 2016.

[96] D. Calderon, M. L. T. Nguyen, A. Mezger, et al., “Landscape of stimulation-responsive chromatin across diverse human immune cells,” Nature Genetics, vol. 51, no. 10, pp. 1494–1505, Oct. 2019.

[97] A. Hassan, A. Pariatamby, A. Ahmed, H. S. Auta, and F. S. Hamid, “Enhanced bioremediation of heavy metal contaminated landfill soil using filamentous fungi consortia: A demonstration of bioaugmentation potential,” Water, Air, & Soil Pollution, vol. 230, no. 9, p. 215, Sep. 2019.

[98] A. Chantarasiri, “Enrichment and identification of phenanthrene-degrading bacteria isolated from the oil-stained engine sediment in the mangrove swamps of Thailand,” Applied Science and Engineering Progress, vol. 14, no. 2, pp. 206–218, doi: 10.14416/j.asep.2020.04.003.

[99] X. Qian, L. Chen, Y. Sui, C. Chen, W. Zhang, J. Zhou, W. Dong, M. Jiang, F. Xin, and K. Ochsenreither, “Biotechnological potential and applications of microbial consortia,” Biotechnology Advances, vol. 40, p. 107500, May 2020.

[100] T. Sumranwanich, K. Boonthaworn, and A. Singh, “The roles of plant cell wall as the first-line protection against lead (Pb) toxicity,” KMUTNB International Journal of Applied Science and Technology, vol. 11, no. 4, pp. 239–245, doi: 10.14416/j.ijast.2018.09.003.

[101] C. C. Azubuike, C. B. Chikere, and G. C. Okpokwasili, “Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects,” World Journal of Microbiology and Biotechnology, vol. 32, no. 11, p. 180, Nov. 2016.

[102] S. Verma and A. Kuila, “Bioremediation of heavy metals by microbial process,” Environmental Technology & Innovation, vol. 14, p. 100369, May 2019.

[103] D. Paul, G. Pandey, J. Pandey, and R. K. Jain, “Accessing microbial diversity for bioremediation and environmental restoration,” Trends in Biotechnology, vol. 23, no. 3, pp. 135–142, Mar. 2005.

[104] E. M. Ramírez, C. S. Jiménez, J. V. Camacho, M. A. R. Rodrigo, and P. Cañizares, “Feasibility of coupling permeable bio-barriers and electrokinetics for the treatment of diesel hydrocarbons polluted soils,” Electrochimica Acta, vol. 181, pp. 192–199, Nov. 2015.

[105] M. Villegas-Plazas, J. Sanabria, and H. Junca, “A composite taxonomical and functional framework of microbiomes under acid mine drainage bioremediation systems,” Journal of Environmental Management, vol. 251, p. 109581, Dec. 2019.

[106] O. Adelaja, T. Keshavarz, and G. Kyazze, “Enhanced biodegradation of phenanthrene using different inoculum types in a microbial fuel cell,” Engineering in Life Sciences, vol. 14, no. 2, pp. 218–228, Mar. 2014.

[107] S. Kim, P. A. Thiessen, E. E. Bolton, J. Chen, G. Fu, A. Gindulyte, L. Han, J. He, S. He, B. A. Shoemaker, J. Wang, B. Yu, J. Zhang, and S. H. Bryant, “PubChem substance and compound databases,” Nucleic Acids Research, vol. 44, no. D1, pp. D1202–D1213, Jan. 2016.

[108] S. Magdouli, S. K. Brar, and J. F. Blais, “Co-culture for lipid production: Advances and challenges,” Biomass and Bioenergy, vol. 92, pp. 20–30, Sep. 2016.

[109] W. Shou, S. Ram, and J. M. G. Vilar, “Synthetic cooperation in engineered yeast populations,” Proceedings of the National Academy of Sciences, vol. 104, no. 6, pp. 1877–1882, Feb. 2007.

[110] U. Suparmaniam, M. K. Lam, Y. Uemura, J. W. Lim, K. T. Lee, and S. H. Shuit, “Insights into the microalgae cultivation technology and harvesting process for biofuel production: A review,” Renewable and Sustainable Energy Reviews, vol. 115, p. 109361, Nov. 2019.

[111] A. Kerner, J. Park, A. Williams, and X. N. Lin, “A programmable escherichia coli consortium via tunable symbiosis,” PLoS ONE, vol. 7, no. 3, p. e34032, Mar. 2012.

[112] J. Fernández-López, J. M. Fernández-Ginés, L. Aleson-Carbonell, E. Sendra, E. Sayas-Barberá, and J. A. Pérez-Alvarez, “Application of functional citrus by-products to meat products,” Trends in Food Science & Technology, vol. 15, no. 3–4, pp. 176– 185, Mar. 2004.

[113] L. Goers, P. Freemont, and K. M. Polizzi, “Co-culture systems and technologies: Taking synthetic biology to the next level,” Journal of The Royal Society Interface, vol. 11, no. 96, p. 20140065, Jul. 2014.

[114] S. Rollié, M. Mangold, and K. Sundmacher, “Designing biological systems: Systems engineering meets synthetic biology,” Chemical Engineering Science, vol. 69, no. 1, pp. 1–29, Feb. 2012.

[115] M. W. I. Schmidt, M. S. Torn, S. Abiven, T. Dittmar, G. Guggenberger, I. A. Janssens, M. Kleber, I. Kögel-Knabner, J. Lehmann, D. A. C. Manning, P. Nannipieri, D. P. Rasse, S. Weiner, and S. E. Trumbore,“Persistence of soil organic matter as an ecosystem property,” Nature, vol. 478, no. 7367, pp. 49–56, Oct. 2011.

[116] B. K. Singh and P. Trivedi, “Microbiome and the future for food and nutrient security,” Microbial Biotechnology, vol. 10, no. 1, pp. 50–53, Jan. 2017.

Full Text: PDF

DOI: 10.14416/j.asep.2021.07.008

Refbacks

There are currently no refbacks.

Username
Password
Remember me