Chapter 10. Using microbial community interactions within plant microbiomes to advance an evergreen agricultural revolution

In: Sustainable agroecosystems in climate change mitigation
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M.E. Lucero
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S. DeBolt
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A. Unc
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A. Ruiz-Font
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L.V. Reyes
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R.L. McCulley
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S.C. Alderman
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R.D. Dinkins
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J.R. Barrow
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D.A. Samac
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Innovative plant breeding and technology transfer fostered the Green Revolution (GR), which transformed agriculture worldwide by increasing grain yields in developing countries. The GR temporarily alleviated world hunger, but also reduced biodiversity, nutrient cycling, and carbon (C) sequestration that agricultural lands can provide. Meanwhile, economic disparity and food insecurity within and among countries continues. Subsequent agricultural advances, focused on objectives such as increasing crop yields or reducing the risk of a specific pest, have failed to meet food demands at the local scale or to restore lost ecosystem services. An increasing human population, climate change, growing per capita food and energy demands, and reduced ecosystem potential to provide agriculturally relevant services have created an unrelenting need for improved crop production practices. Meeting this need in a sustainable fashion will require interdisciplinary approaches that integrate plant and microbial ecology with efforts to advance crop production while mitigating effects of a changing climate. Metagenomic advances are revealing microbial dynamics that can simultaneously improve crop production and soil restoration while enhancing crop resistance to environmental change. Restoring microbial diversity to contemporary agroecosystems could establish ecosystem services while reducing production costs for agricultural producers. Our framework for examining plant-microbial interactions at multiple scales, modeling outcomes to broadly explore potential impacts, and interacting with extension and training networks to transfer microbial based agricultural technologies across socioeconomic scales, offers an integrated strategy for advancing agroecosystem sustainability while minimizing potential for the kind of negative ecological and socioeconomic feedbacks that have resulted from many widely adopted agricultural technologies.

  • Barrow, J.R., Lucero, M.E., Reyes-Vera, I. and Havstad, K., 2008. Do symbiotic microbes have a role in plant evolution, performance and response to stress? Communicative and Integrative Biology 1: 69-93.

  • Bill and Melinda Gates Foundation, 2009. Global development program fact sheet, Bill & Melinda Gates Foundation. Available at: http://www.gatesfoundation.org/about/Documents/GlobalDevelopmentProgramFactSheet.pdf.

  • Borlaug, N.E., 1977. The green revolution: can we make it meet expectations? Proceedings of the American Phytopathological Society 3: 6-21.

  • Borlaug, N.E. and Aresvik, O.H., 1973. The green revolution-an approach to agricultural development and some of its economic implications. International Journal of Agrarian Affairs 4: 385-402.

  • Briggs, A.L. and Morgan, J.W., 2012. Post-cultivation recovery of biological soil crusts in semi-arid native grasslands, southern Australia. Journal of Arid Environments 77: 84-89.

  • Bueno, C.S. and Ladha, J.K., 2009. Comparison of soil properties between continuously cultivated and adjacent uncultivated soils in rice-based systems. Biology and Fertility of Soils 45: 499-509.

  • Carlson, L., 2005. Forging his own path: William Jasper Spillman and progressive era breeding and genetics. Agricultural History 79: 50-73.

  • Committee on Metagenomics: challenges and functional applications, National Research Council, 2007. The new science of metagenomics: revealing the secrets of our microbial planet. The National Academies Press, Washington, DC, USA. Available at: http://www.nap.edu/openbook.php?record_id=11902.

  • Couch, B.C., Fudal, I., Lebrun, M.H., Tharreau, D., Valent, B., Van Kim, P., Nottéghem, J.L. and Kohn, L.M., 2005. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170: 613-630.

  • Das, R.J., 2002. The green revolution and poverty: a theoretical and empirical examination of the relation between technology and society. Geoforum 33: 55-72.

  • Doebley, J., Gaut, B. and Smith, B., 2006. The molecular genetics of crop domestication. Cell 127: 1309-1321.

  • Dubey, A. and Lal, R., 2009. Carbon footprint and sustainability of agricultural production systems in Punjab, India, and Ohio, USA. Journal of Crop Improvement 23: 332-350.

  • Evans, R.D. and Belnap, J., 1999. Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80: 150-160.

  • Eyre-Walker, A., Gaut, R.L., Hilton, H., Feldman, D.L. and Gaut, B.S., 1998. Investigation of the bottleneck leading to the domestication of maize. Proceedings of the National Academy of Sciences of the USA 95: 4441-4446.

  • Food and Agriculture Organization (FAO), 2008. High food prices and food security-threats and opportunities, Food and Agriculture Organization of the United Nations, Rome, Italy. Available at: ftp://ftp.fao.org/docrep/fao/011/i0291e/i0291e00.pdf.

  • Food and Agriculture Organization (FAO), 2011. How does international price volatility affect domestic economies and food security? Food and Agriculture Organization of the United Nations, Rome, Italy. Available at: http://www.fao.org/docrep/013/i2050e/i2050e.pdf.

  • Fox, J.E., Burow, M.E., McLachlan, J.A, Gulledte, J. and Engelhaupt, E., 2007. Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proceedings of the National Academy of Sciences of the USA 104: 10282-10287.

  • Frank, B., 2005. On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of A.B. Frank's classic paper of 1885). Mycorrhiza 15: 267-275.

  • Gale, W.J., Cambardella, C.A. and Bailey, T.B., 2000. Root-derived carbon and the formation and stabilization of aggregates. Soil Science Society of America Journal 64: 201-207.

  • Green, L.E., Porras-Alfaro, A., and Sinsabaugh, R.L., 2008. Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. Journal of Ecology 96: 1076-1085.

  • Gunningham, N., 2007. Incentives to improve farm management: EMS, supply-chains and civil society. Journal of Environmental Management 82: 302-310.

  • Khidir, H.H., Eudy, D.M., Porras-Alfaro, A., Herrera, J., Natvig, D. O. and Sinsabaugh, R.L., 2008. A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. Journal of Arid Environments 74: 35-42.

  • Kiers, E.T., Leakey, R.R.B., Izac, A.M., Heinemanen, J.A., Rosenthal, E., Nathan, D. and Jiggins, J., 2008. Ecology: agriculture at a crossroads. Science 320: 320-321.

  • Kuldau, G. and Bacon, C., 2008. Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biological Control 46: 57-71.

  • Lairon, D., 2010. Nutritional quality and safety of organic food. A review. Agronomy for Sustainable Development 30: 33-41.

  • Lee, K., Pan, J.J. and May, G., 2009. Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. FEMS Microbiology Letters 299: 31-37.

  • Lombard, K.A., Forster-Cox, S., Smeal, D. and O’Neill, M.K., 2006. Diabetes on the Navajo nation: what role can gardening and agriculture extension play to reduce it? Rural and Remote Health 6: 640.

  • Lucero, M.E., Unc, A., Cooke, P., Dowd and Sun, S., 2011. Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. Public Library of Science One 6: e17693.

  • Lynch, J.P., 2007. Roots of the second green revolution. Australian Journal of Botany 55: 493-412.

  • Mann, H., 1848. Education and national welfare. Twelfth annual report of horace mann as secretary of Massachusetts State Board of Education. Massachusetts State Board of Education. Available at: http://usa.usembassy.de/etexts/democrac/16.htm.

  • Moran, M.S., Peters, D.P.C., McClaran, M.P., Nichols, M.H. and Adams, M.B., 2008. Long-term data collection at USDA experimental sites for studies of ecohydrology. Ecohydrology 1: 377-393.

  • Müller-Stöver, D., Hauggard-Nielsen, H., Eriksen, J., Ambus, P., and Johansen, A., 2012. Microbial biomass, microbial diversity, soil carbon storage, and stability after incubation of soil from grass-clover pastures of different age. Biology and Fertility of Soils 48: 371-383.

  • Okon, Y., 1985. Azospirillum as a potential inoculant for agriculture. Trends in Biotechnology 3: 223-228.

  • Ortiz, O., 2006. Evolution of agricultural extension and information dissemination in Peru: an historical perspective focusing on potato-related pest control. Agriculture and Human Values 23: 477-489.

  • Ortiz, R., Crouch, J.H., Crossa, J., Crouch, J.H., Crossa, J., Braun, H.J., Dodds, J.H., Trethowan, R., Ferrara, G.O. and Iwanaga, M., 2007. High yield potential, shuttle breeding, genetic diversity, and a new international wheat improvement strategy. Euphytica 157: 365-384.

  • Peters, D.P.C., Pielke, Sr. R.A., Bestelmeyer, B.T., Allen, C.D., Munson-McGee, S. and Havstad, K.M., 2004. Cross-scale interactions, nonlinearities, and forecasting catastrophic events. Proceedings of the National Academy of Sciences USA 101: 15130-15135.

  • Peters, D.P.C., Sala, O.E. and Allen, C.D., 2007. Cascading events in linked ecological and socioeconomic systems. Frontiers in Ecology and the Environment 5: 221-224.

  • Peters, S.J., 2006. Every farmer should be awakened: Liberty Hyde Bailey's vision of agricultural extension work. Agricultural History 80: 190-219.

  • Pinstrup-Anderson, P. and Hazell, P.B.R., 1985. The impact of the green revolution and prospects for the future. Food Reviews International 1: 1-25.

  • Plett, J.M. and Martin, F., 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends in Genetics 27: 14-22.

  • Richardson, A.E., 2001., Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Functional Plant Biology 28: 897-906.

  • Rodriguez, H. and Fraga R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances 17: 319-339.

  • Rodriguez, R. and Redman, R., 2008. More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109-1114.

  • Sanchez, P.A. and Swaminathan, M.S., 2005. Cutting world hunger in half. Science 307: 357-359.

  • Schardl, C.L., Leuchtmann, A. and Spiering, M.J., 2004. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55: 315-340.

  • Stanger, T.F. and Lauer, J.G., 2008. Corn grain yield response to crop rotation and nitrogen over 35 years. Agronomy Journal 100: 643-650.

  • Swaminathan, M., 1968. Presidential address, agricultural science section the age of algeny, genetic destruction of yield barriers and agricultural transformation, Varanasi, 1968.

  • Swaminathan, M.S., 2010. From green to an evergreen revolution, In: Science and sustainable food security: selected papers of MS Swaminathan, World Scientific Publishing Company Pte. Ltd., Singapore, pp. 27-40.

  • UN Millennium Project, 2005. Investing in development: a practical plan to achieve the millennium development goals. Available at: http://www.unmillenniumproject.org/reports/fullreport/htm.

  • UN Millennium Project, Task Force on Science, Technology, and Innovation, 2005. Innovation: applying knowledge in development. New York. Available at: http://www.unmillenniumproject.org/documents/Science-part1.pdf.

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  • Barrow, J.R., Lucero, M.E., Reyes-Vera, I. and Havstad, K., 2008. Do symbiotic microbes have a role in plant evolution, performance and response to stress? Communicative and Integrative Biology 1: 69-93.

  • Bill and Melinda Gates Foundation, 2009. Global development program fact sheet, Bill & Melinda Gates Foundation. Available at: http://www.gatesfoundation.org/about/Documents/GlobalDevelopmentProgramFactSheet.pdf.

  • Borlaug, N.E., 1977. The green revolution: can we make it meet expectations? Proceedings of the American Phytopathological Society 3: 6-21.

  • Borlaug, N.E. and Aresvik, O.H., 1973. The green revolution-an approach to agricultural development and some of its economic implications. International Journal of Agrarian Affairs 4: 385-402.

  • Briggs, A.L. and Morgan, J.W., 2012. Post-cultivation recovery of biological soil crusts in semi-arid native grasslands, southern Australia. Journal of Arid Environments 77: 84-89.

  • Bueno, C.S. and Ladha, J.K., 2009. Comparison of soil properties between continuously cultivated and adjacent uncultivated soils in rice-based systems. Biology and Fertility of Soils 45: 499-509.

  • Carlson, L., 2005. Forging his own path: William Jasper Spillman and progressive era breeding and genetics. Agricultural History 79: 50-73.

  • Committee on Metagenomics: challenges and functional applications, National Research Council, 2007. The new science of metagenomics: revealing the secrets of our microbial planet. The National Academies Press, Washington, DC, USA. Available at: http://www.nap.edu/openbook.php?record_id=11902.

  • Couch, B.C., Fudal, I., Lebrun, M.H., Tharreau, D., Valent, B., Van Kim, P., Nottéghem, J.L. and Kohn, L.M., 2005. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170: 613-630.

  • Das, R.J., 2002. The green revolution and poverty: a theoretical and empirical examination of the relation between technology and society. Geoforum 33: 55-72.

  • Doebley, J., Gaut, B. and Smith, B., 2006. The molecular genetics of crop domestication. Cell 127: 1309-1321.

  • Dubey, A. and Lal, R., 2009. Carbon footprint and sustainability of agricultural production systems in Punjab, India, and Ohio, USA. Journal of Crop Improvement 23: 332-350.

  • Evans, R.D. and Belnap, J., 1999. Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80: 150-160.

  • Eyre-Walker, A., Gaut, R.L., Hilton, H., Feldman, D.L. and Gaut, B.S., 1998. Investigation of the bottleneck leading to the domestication of maize. Proceedings of the National Academy of Sciences of the USA 95: 4441-4446.

  • Food and Agriculture Organization (FAO), 2008. High food prices and food security-threats and opportunities, Food and Agriculture Organization of the United Nations, Rome, Italy. Available at: ftp://ftp.fao.org/docrep/fao/011/i0291e/i0291e00.pdf.

  • Food and Agriculture Organization (FAO), 2011. How does international price volatility affect domestic economies and food security? Food and Agriculture Organization of the United Nations, Rome, Italy. Available at: http://www.fao.org/docrep/013/i2050e/i2050e.pdf.

  • Fox, J.E., Burow, M.E., McLachlan, J.A, Gulledte, J. and Engelhaupt, E., 2007. Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proceedings of the National Academy of Sciences of the USA 104: 10282-10287.

  • Frank, B., 2005. On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of A.B. Frank's classic paper of 1885). Mycorrhiza 15: 267-275.

  • Gale, W.J., Cambardella, C.A. and Bailey, T.B., 2000. Root-derived carbon and the formation and stabilization of aggregates. Soil Science Society of America Journal 64: 201-207.

  • Green, L.E., Porras-Alfaro, A., and Sinsabaugh, R.L., 2008. Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. Journal of Ecology 96: 1076-1085.

  • Gunningham, N., 2007. Incentives to improve farm management: EMS, supply-chains and civil society. Journal of Environmental Management 82: 302-310.

  • Khidir, H.H., Eudy, D.M., Porras-Alfaro, A., Herrera, J., Natvig, D. O. and Sinsabaugh, R.L., 2008. A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. Journal of Arid Environments 74: 35-42.

  • Kiers, E.T., Leakey, R.R.B., Izac, A.M., Heinemanen, J.A., Rosenthal, E., Nathan, D. and Jiggins, J., 2008. Ecology: agriculture at a crossroads. Science 320: 320-321.

  • Kuldau, G. and Bacon, C., 2008. Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biological Control 46: 57-71.

  • Lairon, D., 2010. Nutritional quality and safety of organic food. A review. Agronomy for Sustainable Development 30: 33-41.

  • Lee, K., Pan, J.J. and May, G., 2009. Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. FEMS Microbiology Letters 299: 31-37.

  • Lombard, K.A., Forster-Cox, S., Smeal, D. and O’Neill, M.K., 2006. Diabetes on the Navajo nation: what role can gardening and agriculture extension play to reduce it? Rural and Remote Health 6: 640.

  • Lucero, M.E., Unc, A., Cooke, P., Dowd and Sun, S., 2011. Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. Public Library of Science One 6: e17693.

  • Lynch, J.P., 2007. Roots of the second green revolution. Australian Journal of Botany 55: 493-412.

  • Mann, H., 1848. Education and national welfare. Twelfth annual report of horace mann as secretary of Massachusetts State Board of Education. Massachusetts State Board of Education. Available at: http://usa.usembassy.de/etexts/democrac/16.htm.

  • Moran, M.S., Peters, D.P.C., McClaran, M.P., Nichols, M.H. and Adams, M.B., 2008. Long-term data collection at USDA experimental sites for studies of ecohydrology. Ecohydrology 1: 377-393.

  • Müller-Stöver, D., Hauggard-Nielsen, H., Eriksen, J., Ambus, P., and Johansen, A., 2012. Microbial biomass, microbial diversity, soil carbon storage, and stability after incubation of soil from grass-clover pastures of different age. Biology and Fertility of Soils 48: 371-383.

  • Okon, Y., 1985. Azospirillum as a potential inoculant for agriculture. Trends in Biotechnology 3: 223-228.

  • Ortiz, O., 2006. Evolution of agricultural extension and information dissemination in Peru: an historical perspective focusing on potato-related pest control. Agriculture and Human Values 23: 477-489.

  • Ortiz, R., Crouch, J.H., Crossa, J., Crouch, J.H., Crossa, J., Braun, H.J., Dodds, J.H., Trethowan, R., Ferrara, G.O. and Iwanaga, M., 2007. High yield potential, shuttle breeding, genetic diversity, and a new international wheat improvement strategy. Euphytica 157: 365-384.

  • Peters, D.P.C., Pielke, Sr. R.A., Bestelmeyer, B.T., Allen, C.D., Munson-McGee, S. and Havstad, K.M., 2004. Cross-scale interactions, nonlinearities, and forecasting catastrophic events. Proceedings of the National Academy of Sciences USA 101: 15130-15135.

  • Peters, D.P.C., Sala, O.E. and Allen, C.D., 2007. Cascading events in linked ecological and socioeconomic systems. Frontiers in Ecology and the Environment 5: 221-224.

  • Peters, S.J., 2006. Every farmer should be awakened: Liberty Hyde Bailey's vision of agricultural extension work. Agricultural History 80: 190-219.

  • Pinstrup-Anderson, P. and Hazell, P.B.R., 1985. The impact of the green revolution and prospects for the future. Food Reviews International 1: 1-25.

  • Plett, J.M. and Martin, F., 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends in Genetics 27: 14-22.

  • Richardson, A.E., 2001., Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Functional Plant Biology 28: 897-906.

  • Rodriguez, H. and Fraga R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances 17: 319-339.

  • Rodriguez, R. and Redman, R., 2008. More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109-1114.

  • Sanchez, P.A. and Swaminathan, M.S., 2005. Cutting world hunger in half. Science 307: 357-359.

  • Schardl, C.L., Leuchtmann, A. and Spiering, M.J., 2004. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55: 315-340.

  • Stanger, T.F. and Lauer, J.G., 2008. Corn grain yield response to crop rotation and nitrogen over 35 years. Agronomy Journal 100: 643-650.

  • Swaminathan, M., 1968. Presidential address, agricultural science section the age of algeny, genetic destruction of yield barriers and agricultural transformation, Varanasi, 1968.

  • Swaminathan, M.S., 2010. From green to an evergreen revolution, In: Science and sustainable food security: selected papers of MS Swaminathan, World Scientific Publishing Company Pte. Ltd., Singapore, pp. 27-40.

  • UN Millennium Project, 2005. Investing in development: a practical plan to achieve the millennium development goals. Available at: http://www.unmillenniumproject.org/reports/fullreport/htm.

  • UN Millennium Project, Task Force on Science, Technology, and Innovation, 2005. Innovation: applying knowledge in development. New York. Available at: http://www.unmillenniumproject.org/documents/Science-part1.pdf.

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