Award Abstract # 1701918
DISSERTATION RESEARCH: The Evolution of Plant Drought Tolerance and Gene Function Across Historic Frequency Gradients

NSF Org: DEB
Division Of Environmental Biology
Recipient: COLORADO STATE UNIVERSITY
Initial Amendment Date: February 10, 2017
Latest Amendment Date: February 10, 2017
Award Number: 1701918
Award Instrument: Standard Grant
Program Manager: Samuel Scheiner
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: June 1, 2017
End Date: May 31, 2019 (Estimated)
Total Intended Award Amount: $19,760.00
Total Awarded Amount to Date: $19,760.00
Funds Obligated to Date: FY 2017 = $19,760.00
History of Investigator:
  • John McKay (Principal Investigator)
    jkmckay@colostate.edu
  • Grey Monroe (Co-Principal Investigator)
Recipient Sponsored Research Office: Colorado State University
601 S HOWES ST
FORT COLLINS
CO  US  80521-2807
(970)491-6355
Sponsor Congressional District: 02
Primary Place of Performance: Colorado State University
200 W. Lake Street
Fort Collins
CO  US  80521-4593
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): LT9CXX8L19G1
Parent UEI:
NSF Program(s): EVOLUTIONARY GENETICS
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s):
Program Element Code(s): 737800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

This research will investigate the function of genes possibly involved in drought adaptation in wild populations of the plant Arabidopsis thaliana. Droughts are one of nature?s most devastating forces, affecting millions of people each year. Yet as agents of strong selection on plant populations, they are also valuable for understanding basic evolutionary processes, such as discovering the genes involved in adaptation. Furthermore, studying plant evolution in the context of drought may produce the critical knowledge needed to develop drought tolerant crops. Using a global map of historic drought frequency based on remote sensing data, populations were identified that experience very different drought frequencies. From data on genetic differences among those populations, 20 genes were identified that will be studied for their molecular and phenotypic effects. This work is expected to yield key insight into the evolution of gene function, and to confirm genes underlying drought tolerance traits. The results of studying these genes may be of great value to breeding programs working to improve drought tolerance in crop species. In addition, the project will involve mentoring both undergraduate and high school students, including individuals from groups that are underrepresented in the sciences.

Historic drought frequency significantly predicts important drought tolerance traits, flowering time and water use efficiency, among natural accessions of Arabidopsis thaliana. The project will investigate the effects of loss of function alleles on 20 genes involved in flowering time or water use efficiency. A reverse genetics approach based on T-DNA gene knockouts will be used to artificially induce mutations in these genes in a common genomic background. The project will quantify the effect sizes of these hypothesized genes on flowering time and water use efficiency. It will also characterize effects on whole genome expression profiles and abiotic signaling cascades using RNAseq.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Baggs, Erin L. and Monroe, J. Grey and Thanki, Anil S. and OGrady, Ruby and Schudoma, Christian and Haerty, Wilfried and Krasileva, Ksenia V. "Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response" The Plant Cell , v.32 , 2020 https://doi.org/10.1105/tpc.19.00903 Citation Details
Monroe, J. Grey and Gill, Brian and Turner, Kathryn G. and McKay, John K. "Drought regimens predict life history strategies in Heliophila" New Phytologist , 2019 10.1111/nph.15919 Citation Details
Monroe, J Grey and Powell, Tyler and Price, Nicholas and Mullen, Jack L and Howard, Anne and Evans, Kyle and Lovell, John T and McKay, John K "Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function" eLife , v.7 , 2018 10.7554/eLife.41038 Citation Details
Togninalli, Matteo and Seren, Ümit and Freudenthal, Jan A and Monroe, J Grey and Meng, Dazhe and Nordborg, Magnus and Weigel, Detlef and Borgwardt, Karsten and Korte, Arthur and Grimm, Dominik G "AraPheno and the AraGWAS Catalog 2020: a major database update including RNA-Seq and knockout mutation data for Arabidopsis thaliana" Nucleic Acids Research , 2019 10.1093/nar/gkz925 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.

Understanding how plants adapt to drought is critical for crop improvement in the face of rapid climate change and important for understanding the evolution of species in the wild. This project combined computational and experimental innovations to investigate the functional genomics and evolutionary ecology of drought adaptation.

We found evidence that widespread genetic loss-of-function can play an important role in the evolution of drought adaptation in plants. These findings further challenge prior assumptions about the molecular basis of adaptation with important implications for theoretical and applied genetics. Specifically, they indicate that parallel molecular evolution, which is common for genes exhibiting loss-of-function, may play a previously underappreciated role in adaptive evolution. This calls for a reconsideration of the tools used to detect genes involved in the evolution of natural populations and crops. This work presents a broadly scalable framework using whole genome sequence data to identify functionally definitive gene variants affecting phenotypes and experiencing selection. It also highlights the importance of combining population genetics with experimental validation to test hypotheses about gene functional evolution.

The results of this research inspire new opportunities in agriculture for engineering climate resilience in crops. Specifically, they suggest that targeted gene knockouts using emerging technologies may be particularly valuable for directed molecular breeding. These findings have implications for public attitudes toward genetically engineered crops, revealing that knockout mutations can be a natural source of beneficial genetic variation, in contrast to assumptions that gene knockouts are necessarily deleterious.

This work also pioneered the use of remotely sensed drought to scale up the study of the climatic drivers of plant adaptation. These investigations demonstrate the value of using allele environment associations to identify candidate loci associated with phenotypes directly. Specifically, we find that allele associations with drought timing measured using remote sensing technology strongly predict allele associations with flowering time. We also show that remotely sensed drought is an effective tool for predicting broader patterns of trait variation by applying it to test classic hypotheses about annual and perennial life history strategies in relation to drought. We find support, for the first time in a phylogenetic comparative analysis, for the classic prediction that annual species should occur in environments where droughts are frequent and predictable. Thus, this work reveals the importance of drought regimens to predict adaptive traits in plants.

The results from this work have been published in eLife, New Phytologist and the PhD dissertation of PI Monroe, with the publication in eLife receiving additional attention with a F1000Prime recommendation. This grant has also supported work included in several manuscripts currently being prepared for submission. PI Monroe presented this research at the international Evolution conference in 2017. He was also invited to give research seminars presenting work supported by this grant at Appalachian State University, Duke University, the International Rice Research Institute, Australian National University, Colorado State University, The Max Planck Institute for Developmental Biology, The Max Planck Institute for Plant Breeding, The University of Cologne, The International Center for Tropical Agriculture, and the University of California Davis.

This project resulted in undergraduate mentorship and authorship for contributions made. Additionally, while conducting this research, PI Monroe participated in an initiative called Research Mentoring to Advance Inclusivity in STEM.  This program provided training and the development of lesson plans to teach peers and their mentees about implicit bias. 

 


Last Modified: 08/15/2019
Modified by: J. Grey Monroe

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