The Untapped Potential of Plant Microbiomes in Agriculture Jan E. Leach Colorado State University American Society of Plant Biologists American Phytopathological Society Plant Microbiomes: Assemblages of microbes living in, on and around plants Hirsch & Mauchline, Nature Biotech 2012 Plant microbiomes are components of Phytobiomes: . all organisms living in, on and around plants . microbes . animals . other plants . the Environment Phytobiomes initiative focused on agriculture Plant and their microbiomes are partners for LIFE • Plant microbiomes can influence or be influenced by plants or the plant environment • How can that relationship be tapped to improve crop health, safety, quality and productivity? Quality Health Safety Productivity Nutrition Why now? • Advances in systems-level approaches – High-throughput sequencing – Metagenomics & other ‘-omics technologies – Data sciences (data mining, predictive analytics, …) – Computer science (machine learning, image processing and graphics, …) • Human microbiome discoveries – Conserved patterns despite variation – Strength of longitudinal vs cross-sectional studies – Unexpected impacts on the host – Successful translation to treatments (fecal transplants, probiotics) • International microbiomes attention – OSTP process (NSTC report out SOON!) – Unified Initiative (Science, Nature) • Management strategies in agriculture – Precision Ag – Decision support systems Lessons from the human microbiome When Gut Bacteria Changes Brain Function “…. the microbiome may play a role in regulating how people think and feel.” David Kohn The Atlantic June 24, 2015 Chick-fil-a How do we assess microbiomes? Sample collection Community Community RNA, protein, DNA extraction metabolite extraction PCR amplify (16S-18S rRNA, ITS, cpn60) Amplicon Metagenome Meta- Metaproteome Metabolome sequencing sequencing transcriptome analysis analysis sequencing Species (taxa) number, abundance, composition Community function Community activity “Who is there?” “What can they do?” “What are they doing?” Who is there? Bacterial & fungal communities: Census of the it’s complex! microbial communities on distinct tissues of tomato Ottesen et al 2013. BMC Microbiology Do plants control their microbiome composition? • DNA from microbes in the seed, rhizosphere, and endophytic compartments, and soils • amplicon sequencing Johnston-Montje et al, BMC Plant Biol 2014 Lundberg et al, Nature 2012 Bulgarelli et al, Nature 2012 Hirsch et al, Nature Biotech 2012 And others Plants can select microbiome • Plant genotype –dependent selection fine-tunes the internalized microbial Lundberg Nature 2012 community profiles Bulgarelli Nature 2012 • Plants can transmit bacterial endophytes from generation to generation through seed Applications? • Can we breed plants that select for a beneficial microbiome? • Have we inadvertently selected against plant traits that help support Traditionalbeneficial Modern microbes by breeding for high yield under conditions of high inputs and soil tillage? • What is the potential for identifying new, more successful biocontrol agents? Influence of disease on microbiomes? •Rhizosphere microbiome on trees with citrus greening are different from those on uninfected trees Disease is associated with shifts in the microbiome composition Healthy trees Microbiome shifts Infected trees diagnostic for disease Trivedi et al. 2012. ISME J 6:363 Microbiome function provides insights into mechanisms/consequences of disease: • Functional shift: away from use of easily degraded carbon sources to more recalcitrant forms –consistent with carbohydrate repartitioning during citrus greening disease ( photosynthate to roots…) Trivedi et al 2012. ISME J Microbiomes can protect plants against pathogens/pests Plants are subject to infection by diverse microbial pathogens as well as herbivory by insect and nematode pests ► Microbial communities in soils can suppress diseases Mendes et al. 2011 Microbes reduce effects of drought, flooding & salinity Microbes enhance root growth via phytohormone production more and deeper roots Microbes minimize the inhibitory effect of ethylene on plant growth - produce ACC deaminase Microbes form biofilms that reduce ion movement into the plant Dimkpa. 2009. Plant Cell Environ 32:1682 Insects-microbes-plants? PNAS 110:15728 • Bacteria associated with the Colorado potato beetle manipulate plant defenses to facilitate beetle feeding Science (2011) 332:1097Trends Biotech (2012) 30:177 Environ Microbiol (2012) 14:4 Trends Plant Sci (2012) 17: 478 Mol Ecol (2014) 23:1571 Annu Rev Phytopathol (2014) 51:17 Functional soil microbiome: Belowground solutions to an aboveground problem. Laksmanan V1, Selvaraj G1, Bais H2. Plant Physiol 2014 [Epub ahead of print] (2014) Frontiers Microbiol (2014) 5:1 FEMS Microbial Ecol 2011 The Future: • Management strategies that create disease-suppressive microbial communities • Plants that select for and maintain beneficial microbiomes http://www.the-scientist.com/?articles.view/articleNo/33703/title/Fighting-Microbes-with-Microbes/ The Future: • Managed/engineered microbiomes that promote sustained crop productivity – rebuild depleted/degraded soils – produce with less water – produce in changing climate Source: UNEP *1..5 billion people depend on degraded lands for survival! The Future: • Smart microbes that detect and treat disease/destroy pests (Image by Brett Ryder, NewScientist.com) Biota Crop Soil Technology Water Data Weather Raj Khosla, Colorado State University Understanding and application of microbiomes to advance agriculture requires: . Interdisciplinary, systems level approaches . Considertion of interactions in context (the phytobiome) "We have to remember that what we observe is not nature in itself, but nature exposed to our method of questioning." - Werner Heisenberg (Theoretical physicist) Roadmap for Phytobiomes Research and Translation @phytobiomes www.phytobiomes.org • Define vision and strategy • Implementation: – International Consortium – Advocacy for new funding Acknowledgements • The American Society of Plant Biologists • The American Phytopathological Society • Funding sources • APS, Noble Foundation, NSF, USDA-NIFA, US Forest Service, Bayer CropScience, • Phytobiomes Initiative Co-Chairs Gwyn Beattie, Iowa State University Kellye Eversole, Eversole Associates • Phytobiomes Partners @phytobiomes www.phytobiomes.com .