Award Abstract # 1856744
RESEARH-PGR: Genomics of strain- and host-specific performance in the legume-rhizobia symbiosis

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: REGENTS OF THE UNIVERSITY OF MINNESOTA
Initial Amendment Date: July 17, 2019
Latest Amendment Date: August 19, 2021
Award Number: 1856744
Award Instrument: Standard Grant
Program Manager: Shin-Han Shiu
sshiu@nsf.gov
 (792)292-7989
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: August 1, 2019
End Date: July 31, 2024 (Estimated)
Total Intended Award Amount: $1,768,277.00
Total Awarded Amount to Date: $1,768,277.00
Funds Obligated to Date: FY 2019 = $1,768,277.00
History of Investigator:
  • Peter Tiffin (Principal Investigator)
    ptiffin@umn.edu
  • Michael Sadowsky (Co-Principal Investigator)
  • Katy Heath (Co-Principal Investigator)
  • Liana Burghardt (Co-Principal Investigator)
  • Devanshi Khokhani (Co-Principal Investigator)
  • Nevin Young (Former Co-Principal Investigator)
Recipient Sponsored Research Office: University of Minnesota-Twin Cities
2221 UNIVERSITY AVE SE STE 100
MINNEAPOLIS
MN  US  55414-3074
(612)624-5599
Sponsor Congressional District: 05
Primary Place of Performance: University of Minnesota-Twin Cities
1445 Gortner Avenue
St. Paul
MN  US  55108-1095
Primary Place of Performance
Congressional District:
04
Unique Entity Identifier (UEI): KABJZBBJ4B54
Parent UEI:
NSF Program(s): Plant Genome Research Project
Primary Program Source: 01001920DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1329, 7577, 9109, 9178, 9179, BIOT
Program Element Code(s): 132900
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

The plants and animals we see around us, including agriculturally important crop plants, live in close association with millions of microorganisms (microbes). Some of these microbes cause disease but others are beneficial. Identifying the genes and genetic pathways that determine the outcome of host-microbe associations provides targets for manipulating them for human benefit. This project uses an innovative approach based on high-throughput genome sequencing to efficiently identify bacterial and host genes that shape the outcome of host-microbe associations. The new methods are being deployed on one of the most important plant-microbe associations, that between leguminous plants (soybeans, beans, peas, alfalfa) and rhizobial bacteria. When rhizobia grow in association with these plants, they convert atmospheric nitrogen into a plant useable form, thereby "feeding" the plant and lessening the need for nitrogen fertilizer. The results will provide new empirical tools that advance how we study these systems and the identification of genes and bacterial strains that can be exploited to increase the benefits rhizobial bacteria provide in agricultural systems. Teams of student writers and designers, as well as local high school teachers, will be actively involved in the project to communicate the results using print, graphics, and animation.

The symbiosis between leguminous plants and rhizobial bacteria is a classic system for understanding how plant and microbial genomes function in a coordinated manner. The benefits of host-rhizobia interactions depend on genomic variation found in both partners (i.e. inter-genome or genome-by-genome variation). Neither the reasons for nor the consequences of this inter-genome variation are well understood. Moreover, very little is known about the genetic basis of genome by genome variation in this, or any other, host-microbe system. The research under this award will fill this void through a novel two-species genotype-phenotype association study, two-species co-expression networks, and functional validation of candidate genes. A similar approach will be used to evaluate the inter-genome variation between Medicago and Aphanomyces, an economically important pathogen. The data and code used for analyses will be made available in a timely manner through public data repositories. Analyses of these data will uncover, in unprecedented detail, the genetic basis and mechanisms responsible for variation in inter-genome effects on phenotype in host-symbiont and host-pathogen systems. To extend the reach of the project and actively disseminate the results, students from other disciplines (such as writers and graphic designers) will develop new communication materials that will be used in local high school curricula.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Batstone, Rebecca T. and Burghardt, Liana T. and Heath, Katy D. "Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont" Proceedings of the Royal Society B: Biological Sciences , v.289 , 2022 https://doi.org/10.1098/rspb.2022.0477 Citation Details
Batstone, Rebecca T. and Lindgren, Hanna and Allsup, Cassandra M. and Goralka, Laura A. and Riley, Alex B. and Grillo, Michael A. and Marshall-Colon, Amy and Heath, Katy D. "Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes" mBio , v.13 , 2022 https://doi.org/10.1128/mbio.01823-22 Citation Details
Burghardt, Liana T and diCenzo, George C "The evolutionary ecology of rhizobia: multiple facets of competition before, during, and after symbiosis with legumes" Current Opinion in Microbiology , v.72 , 2023 https://doi.org/10.1016/j.mib.2023.102281 Citation Details
Burghardt, Liana T. and Epstein, Brendan and Hoge, Michelle and Trujillo, Diana I. and Tiffin, Peter "Host-Associated Rhizobial Fitness: Dependence on Nitrogen, Density, Community Complexity, and Legume Genotype" Applied and Environmental Microbiology , v.88 , 2022 https://doi.org/10.1128/aem.00526-22 Citation Details
Burghardt, LT and Trujillo, D and Epstein, B and Tiffin, P "Select-and-resequence screening reveals rhizobia strain-specific effects of nodule-specific PLAT domain genes in Medicago truncatula" Plant physiology , 2020 doi: 10.1104/pp.19.00831 Citation Details
Burns, Mannix and Epstein, Brendan and Burghardt, Liana "Comparison of nodule endophyte composition, diversity, and gene content between Medicago truncatula genotypes" Phytobiomes Journal , 2021 https://doi.org/10.1094/PBIOMES-10-20-0077-R Citation Details
Epstein, B and Tiffin, P "Comparative genomics reveals high rates of horizontal transfer and strong purifying selection on rhizobial symbiosis genes" Proceedings , v.288 , 2021 https://doi.org/doi.org/10.1098/rspb.2020.1804 Citation Details
Epstein, Brendan and Burghardt, Liana T. and Heath, Katy D. and Grillo, Michael A. and Kostanecki, Adam and Hämälä, Tuomas and Young, Nevin D. and Tiffin, Peter "Combining GWAS and population genomic analyses to characterize coevolution in a legumerhizobia symbiosis" Molecular Ecology , 2022 https://doi.org/10.1111/mec.16602 Citation Details
Kosmopoulos, James C and Batstone-Doyle, Rebecca T and Heath, Katy D "Co-inoculation with novel nodule-inhabiting bacteria reduces the benefits of legumerhizobium symbiosis" Canadian Journal of Microbiology , v.70 , 2024 https://doi.org/10.1139/cjm-2023-0209 Citation Details
Riley, Alex B. and Grillo, Michael A. and Epstein, Brendan and Tiffin, Peter and Heath, Katy D. "Discordant population structure among rhizobium divided genomes and their legume hosts" Molecular Ecology , v.32 , 2022 https://doi.org/10.1111/mec.16704 Citation Details

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The plants and animals we see live in close relationships with microbes (organisms that are too small for us to see without a microscope).  Most of these microbes have no effect on plant or animal health or growth, some cause disease, and a few are mutualists that promote plant growth and animal health.  Understanding mutualisms not only provides insight into how plants regulate the bacteria that live with them but also may provide tools we can use to manipulate them for our benefit.

One of the most important plant-bacteria mutualism occurs between legume plants (beans, peas, alfalfa) and Sinorhizobia bacteria; when living inside of the plant Sinorhizobia bacteria convert atmospheric nitrogen into a form the plants can use as fertilizer, a process known as nitrogen fixation.  Nitrogen fixation can greatly limit the need for nitrogen fertilizers in agricultural settings.  The overall objective of this project was to identify which plant and which bacteria genes determine the amount of nitrogen fixation, and thus the net benefit, that benefits that plants obtain from these mutualistic bacteria.

Using an innovative experimental approach and genomic analyses, we replicated earlier work showing that variation among bacterial strains has important consequences for the outcome of legume-bacteria mutualism and we also identified genes in both plants and in bacteria that are directly involved in the benefits host-specific benefits. These genes provide insight into the mechanisms plants use to regulate the microbes that live with them.  These genes also provide candidates that could be targeted by genomic manipulation to improve nitrogen fixation in agricultural crops. We also applied our experimental approach to a plant (corn) -pathogen system to learn more about the importance of strain variation in the outcomes of plant disease.

We communicated our findings to other researchers through presentations at scientific conferences and workshops and through publications in peer-reviewed journals.  We made all the data we collected for this project publicly available.

Beyond advancing our understanding of the genetics of plant-bacteria mutualisms, our project supported training opportunities for undergraduate students, graduate students, and advanced researchers (postdoctoral scholars).  All trainees learned more about science.  Several of them have gone on to science-based jobs in the private sector, academic positions, or further education in science.  We also collaborated with a high school teacher to develop hands-on science activities for high school students, and we participated in community activities that promote science and science education. 

 


Last Modified: 10/01/2024
Modified by: Peter L Tiffin

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