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Title: The genomic landscape of molecular responses to natural drought stress in Panicum hallii

Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.
Authors:
 [1] ; ORCiD logo [2] ;  [3] ; ORCiD logo [2] ; ORCiD logo [2] ;  [4] ;  [5] ;  [4] ;  [4] ;  [5] ; ORCiD logo [6] ;  [3] ;  [4] ;  [5] ; ORCiD logo [4] ; ORCiD logo [4] ;  [2] ;  [7] ; ORCiD logo [5] ;  [5] more »;  [5] ;  [8] ;  [8] ;  [9] ;  [2] ; ORCiD logo [10] ;  [4] « less
  1. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); The Univ. of Texas, Austin, TX (United States)
  2. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
  3. Michigan State Univ., East Lansing, MI (United States)
  4. The Univ. of Texas, Austin, TX (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Zymergen Inc, Emeryville, CA (United States)
  7. The Univ. of Texas, Austin, TX (United States); Kazan Federal University, Kazan (Russia)
  8. Univ. of Arizona, Tucson, AZ (United States)
  9. Univ. of California, Berkeley, CA (United States)
  10. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Grant/Contract Number:
SC0018409
Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Research Org:
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; adaptation; cis; trans; eQTL; plasticity; GxE; compensatory evolution
OSTI Identifier:
1506428

Lovell, John T., Jenkins, Jerry, Lowry, David B., Mamidi, Sujan, Sreedasyam, Avinash, Weng, Xiaoyu, Barry, Kerrie, Bonnette, Jason, Campitelli, Brandon, Daum, Chris, Gordon, Sean P., Gould, Billie A., Khasanova, Albina, Lipzen, Anna, MacQueen, Alice, Palacio-Mejía, Juan Diego, Plott, Christopher, Shakirov, Eugene V., Shu, Shengqiang, Yoshinaga, Yuko, Zane, Matt, Kudrna, Dave, Talag, Jason D., Rokhsar, Daniel, Grimwood, Jane, Schmutz, Jeremy, and Juenger, Thomas E.. The genomic landscape of molecular responses to natural drought stress in Panicum hallii. United States: N. p., Web. doi:10.1038/s41467-018-07669-x.
Lovell, John T., Jenkins, Jerry, Lowry, David B., Mamidi, Sujan, Sreedasyam, Avinash, Weng, Xiaoyu, Barry, Kerrie, Bonnette, Jason, Campitelli, Brandon, Daum, Chris, Gordon, Sean P., Gould, Billie A., Khasanova, Albina, Lipzen, Anna, MacQueen, Alice, Palacio-Mejía, Juan Diego, Plott, Christopher, Shakirov, Eugene V., Shu, Shengqiang, Yoshinaga, Yuko, Zane, Matt, Kudrna, Dave, Talag, Jason D., Rokhsar, Daniel, Grimwood, Jane, Schmutz, Jeremy, & Juenger, Thomas E.. The genomic landscape of molecular responses to natural drought stress in Panicum hallii. United States. doi:10.1038/s41467-018-07669-x.
Lovell, John T., Jenkins, Jerry, Lowry, David B., Mamidi, Sujan, Sreedasyam, Avinash, Weng, Xiaoyu, Barry, Kerrie, Bonnette, Jason, Campitelli, Brandon, Daum, Chris, Gordon, Sean P., Gould, Billie A., Khasanova, Albina, Lipzen, Anna, MacQueen, Alice, Palacio-Mejía, Juan Diego, Plott, Christopher, Shakirov, Eugene V., Shu, Shengqiang, Yoshinaga, Yuko, Zane, Matt, Kudrna, Dave, Talag, Jason D., Rokhsar, Daniel, Grimwood, Jane, Schmutz, Jeremy, and Juenger, Thomas E.. 2018. "The genomic landscape of molecular responses to natural drought stress in Panicum hallii". United States. doi:10.1038/s41467-018-07669-x. https://www.osti.gov/servlets/purl/1506428.
@article{osti_1506428,
title = {The genomic landscape of molecular responses to natural drought stress in Panicum hallii},
author = {Lovell, John T. and Jenkins, Jerry and Lowry, David B. and Mamidi, Sujan and Sreedasyam, Avinash and Weng, Xiaoyu and Barry, Kerrie and Bonnette, Jason and Campitelli, Brandon and Daum, Chris and Gordon, Sean P. and Gould, Billie A. and Khasanova, Albina and Lipzen, Anna and MacQueen, Alice and Palacio-Mejía, Juan Diego and Plott, Christopher and Shakirov, Eugene V. and Shu, Shengqiang and Yoshinaga, Yuko and Zane, Matt and Kudrna, Dave and Talag, Jason D. and Rokhsar, Daniel and Grimwood, Jane and Schmutz, Jeremy and Juenger, Thomas E.},
abstractNote = {Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.},
doi = {10.1038/s41467-018-07669-x},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {12}
}

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