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Title: QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient

Abstract

Local adaptation is the process by which natural selection drives adaptive phenotypic divergence across environmental gradients. Theory suggests that local adaptation results from genetic trade-offs at individual genetic loci, where adaptation to one set of environmental conditions results in a cost to fitness in alternative environments. However, the degree to which there are costs associated with local adaptation is poorly understood because most of these experiments rely on two-site reciprocal transplant experiments. Here, we quantify the benefits and costs of locally adaptive loci across 17° of latitude in a four-grandparent outbred mapping population in outcrossing switchgrass (Panicum virgatumL.), an emerging biofuel crop and dominant tallgrass species. We conducted quantitative trait locus (QTL) mapping across 10 sites, ranging from Texas to South Dakota. This analysis revealed that beneficial biomass (fitness) QTL generally incur minimal costs when transplanted to other field sites distributed over a large climatic gradient over the 2 y of our study. Therefore, locally advantageous alleles could potentially be combined across multiple loci through breeding to create high-yielding regionally adapted cultivars.

Authors:
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Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Texas, Austin, TX (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation Plant Genome Research Program Award
Contributing Org.:
Only Michigan State University received funding directly by this grant for this publication.
OSTI Identifier:
1525532
Alternate Identifier(s):
OSTI ID: 1572023; OSTI ID: 1593753
Grant/Contract Number:  
AC02-05CH11231; SC0014156; SC0017883; SC0018409; FC02-07ER64494
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 26; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bioenergy; ecotype; local adaptation; plasticity; G x E

Citation Formats

Lowry, David B., Lovell, John T., Zhang, Li, Bonnette, Jason, Fay, Philip A., Mitchell, Robert B., Lloyd-Reilley, John, Boe, Arvid R., Wu, Yanqi, Rouquette, Jr, Francis M., Wynia, Richard L., Weng, Xiaoyu, Behrman, Kathrine D., Healey, Adam, Barry, Kerrie, Lipzen, Anna, Bauer, Diane, Sharma, Aditi, Jenkins, Jerry, Schmutz, Jeremy, Fritschi, Felix B., and Juenger, Thomas E. QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient. United States: N. p., 2019. Web. doi:10.1073/pnas.1821543116.
Lowry, David B., Lovell, John T., Zhang, Li, Bonnette, Jason, Fay, Philip A., Mitchell, Robert B., Lloyd-Reilley, John, Boe, Arvid R., Wu, Yanqi, Rouquette, Jr, Francis M., Wynia, Richard L., Weng, Xiaoyu, Behrman, Kathrine D., Healey, Adam, Barry, Kerrie, Lipzen, Anna, Bauer, Diane, Sharma, Aditi, Jenkins, Jerry, Schmutz, Jeremy, Fritschi, Felix B., & Juenger, Thomas E. QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient. United States. https://doi.org/10.1073/pnas.1821543116
Lowry, David B., Lovell, John T., Zhang, Li, Bonnette, Jason, Fay, Philip A., Mitchell, Robert B., Lloyd-Reilley, John, Boe, Arvid R., Wu, Yanqi, Rouquette, Jr, Francis M., Wynia, Richard L., Weng, Xiaoyu, Behrman, Kathrine D., Healey, Adam, Barry, Kerrie, Lipzen, Anna, Bauer, Diane, Sharma, Aditi, Jenkins, Jerry, Schmutz, Jeremy, Fritschi, Felix B., and Juenger, Thomas E. Mon . "QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient". United States. https://doi.org/10.1073/pnas.1821543116.
@article{osti_1525532,
title = {QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient},
author = {Lowry, David B. and Lovell, John T. and Zhang, Li and Bonnette, Jason and Fay, Philip A. and Mitchell, Robert B. and Lloyd-Reilley, John and Boe, Arvid R. and Wu, Yanqi and Rouquette, Jr, Francis M. and Wynia, Richard L. and Weng, Xiaoyu and Behrman, Kathrine D. and Healey, Adam and Barry, Kerrie and Lipzen, Anna and Bauer, Diane and Sharma, Aditi and Jenkins, Jerry and Schmutz, Jeremy and Fritschi, Felix B. and Juenger, Thomas E.},
abstractNote = {Local adaptation is the process by which natural selection drives adaptive phenotypic divergence across environmental gradients. Theory suggests that local adaptation results from genetic trade-offs at individual genetic loci, where adaptation to one set of environmental conditions results in a cost to fitness in alternative environments. However, the degree to which there are costs associated with local adaptation is poorly understood because most of these experiments rely on two-site reciprocal transplant experiments. Here, we quantify the benefits and costs of locally adaptive loci across 17° of latitude in a four-grandparent outbred mapping population in outcrossing switchgrass (Panicum virgatumL.), an emerging biofuel crop and dominant tallgrass species. We conducted quantitative trait locus (QTL) mapping across 10 sites, ranging from Texas to South Dakota. This analysis revealed that beneficial biomass (fitness) QTL generally incur minimal costs when transplanted to other field sites distributed over a large climatic gradient over the 2 y of our study. Therefore, locally advantageous alleles could potentially be combined across multiple loci through breeding to create high-yielding regionally adapted cultivars.},
doi = {10.1073/pnas.1821543116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 26,
volume = 116,
place = {United States},
year = {Mon Jun 10 00:00:00 EDT 2019},
month = {Mon Jun 10 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1821543116

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Works referenced in this record:

Characterization of the Rust Fungus, Puccinia emaculata, and Evaluation of Genetic Variability for Rust Resistance in Switchgrass Populations
journal, October 2012

  • Uppalapati, Srinivasa Rao; Serba, Desalegn D.; Ishiga, Yasuhiro
  • BioEnergy Research, Vol. 6, Issue 2
  • DOI: 10.1007/s12155-012-9263-6

Bmp4 and Morphological Variation of Beaks in Darwin's Finches
journal, September 2004


The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass ( Panicum virgatum)
journal, September 2016

  • Milano, Elizabeth R.; Lowry, David B.; Juenger, Thomas E.
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 11
  • DOI: 10.1534/g3.116.032763

The statistical analysis of multi-environment data: modeling genotype-by-environment interaction and its genetic basis
journal, January 2013

  • Malosetti, Marcos; Ribaut, Jean-Marcel; van Eeuwijk, Fred A.
  • Frontiers in Physiology, Vol. 4
  • DOI: 10.3389/fphys.2013.00044

Extensive Genetic Diversity is Present within North American Switchgrass Germplasm
journal, January 2018


Linking a mutation to survival in wild mice
journal, January 2019

  • Barrett, Rowan D. H.; Laurent, Stefan; Mallarino, Ricardo
  • Science, Vol. 363, Issue 6426
  • DOI: 10.1126/science.aav3824

Evidence for Ecological Speciation and Its Alternative
journal, February 2009


Best Linear Unbiased Estimation and Prediction under a Selection Model
journal, June 1975


Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


Improved experimental protocols to evaluate cold tolerance thresholds in Miscanthus and switchgrass rhizomes
journal, January 2016

  • Peixoto, Murilo de Melo; Sage, Rowan F.
  • GCB Bioenergy, Vol. 8, Issue 2
  • DOI: 10.1111/gcbb.12301

Switchgrass Breeding, Genetics, and Genomics
book, January 2012


Latitudinal and Longitudinal Adaptation of Switchgrass Populations
journal, January 2007


Latitudinal Adaptation of Switchgrass Populations
journal, January 2004


An Overview of the Global Historical Climatology Network-Daily Database
journal, July 2012

  • Menne, Matthew J.; Durre, Imke; Vose, Russell S.
  • Journal of Atmospheric and Oceanic Technology, Vol. 29, Issue 7
  • DOI: 10.1175/JTECH-D-11-00103.1

Perennial Biomass Grasses and the Mason–Dixon Line: Comparative Productivity across Latitudes in the Southern Great Plains
journal, September 2012


Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana
journal, December 2013

  • Agren, J.; Oakley, C. G.; McKay, J. K.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 52
  • DOI: 10.1073/pnas.1316773110

R/qtl: QTL mapping in experimental crosses
journal, May 2003


A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern
journal, July 2006

  • Hoekstra, Hopi E.; Hirschmann, Rachel J.; Bundey, Richard A.
  • Science, Vol. 313, Issue 5783
  • DOI: 10.1126/science.1126121

Modern Applied Statistics with S
book, August 2002


Polyploidy and Winter Survival in Panicum virgatum L.1
journal, January 1947


Genotypic variation in traits linked to climate and aboveground productivity in a widespread C 4 grass: evidence for a functional trait syndrome
journal, May 2013

  • Aspinwall, Michael J.; Lowry, David B.; Taylor, Samuel H.
  • New Phytologist, Vol. 199, Issue 4
  • DOI: 10.1111/nph.12341

Ecological genomics of local adaptation
journal, October 2013

  • Savolainen, Outi; Lascoux, Martin; Merilä, Juha
  • Nature Reviews Genetics, Vol. 14, Issue 11
  • DOI: 10.1038/nrg3522

Population genomic variation reveals roles of history, adaptation and ploidy in switchgrass
journal, July 2014

  • Grabowski, Paul P.; Morris, Geoffrey P.; Casler, Michael D.
  • Molecular Ecology, Vol. 23, Issue 16
  • DOI: 10.1111/mec.12845

Switchgrass Germplasm Resources
journal, January 2015


VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing
journal, February 2012


Reduction of Ethanol Yield from Switchgrass Infected with Rust Caused by Puccinia emaculata
journal, October 2015

  • Sykes, Virginia R.; Allen, Fred L.; Mielenz, Jonathan R.
  • BioEnergy Research, Vol. 9, Issue 1
  • DOI: 10.1007/s12155-015-9680-4

Conceptual issues in local adaptation
journal, December 2004


Conducting Meta-Analyses in R with the metafor Package
journal, January 2010


Mapping mendelian factors underlying quantitative traits using RFLP linkage maps.
journal, January 1989


Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation
journal, June 2017

  • Wadgymar, Susana M.; Lowry, David B.; Gould, Billie A.
  • Methods in Ecology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1111/2041-210X.12777

Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum
journal, May 2014

  • Lowry, David B.; Behrman, Kathrine D.; Grabowski, Paul
  • The American Naturalist, Vol. 183, Issue 5
  • DOI: 10.1086/675760

bnstruct: an R package for Bayesian Network structure learning in the presence of missing data
journal, December 2016


Genomics of local adaptation with gene flow
journal, April 2016

  • Tigano, Anna; Friesen, Vicki L.
  • Molecular Ecology, Vol. 25, Issue 10
  • DOI: 10.1111/mec.13606

Testing for local adaptation in Avena barbata : a classic example of ecotypic divergence
journal, September 2009


C 4 bioenergy crops for cool climates, with special emphasis on perennial C 4 grasses
journal, April 2015

  • Sage, Rowan F.; de Melo Peixoto, Murilo; Friesen, Patrick
  • Journal of Experimental Botany, Vol. 66, Issue 14
  • DOI: 10.1093/jxb/erv123

Plant Mortality and Natural Selection May Increase Biomass Yield in Switchgrass Swards
journal, January 2013


Ecological speciation: Ecological speciation
journal, January 2005


TSPmap, a tool making use of traveling salesperson problem solvers in the efficient and accurate construction of high-density genetic linkage maps
journal, December 2017


Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers
journal, November 2003


A Map of Local Adaptation in Arabidopsis thaliana
journal, October 2011


The Theoretical Population Genetics of Variable Selection and Migration
journal, December 1976


Genetic trade-offs and conditional neutrality contribute to local adaptation: GENETIC BASIS OF LOCAL ADAPTATION
journal, March 2012


Genetic Equilibrium When More Than One Ecological Niche is Available
journal, September 1953

  • Levene, Howard
  • The American Naturalist, Vol. 87, Issue 836
  • DOI: 10.1086/281792

Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana
journal, April 2018

  • Price, Nicholas; Moyers, Brook T.; Lopez, Lua
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 19
  • DOI: 10.1073/pnas.1719998115

Genome-Assisted Prediction of Quantitative Traits Using the R Package sommer
journal, June 2016


Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data
journal, July 2016

  • Grabowski, Paul P.; Evans, Joseph; Daum, Chris
  • New Phytologist, Vol. 213, Issue 1
  • DOI: 10.1111/nph.14101

Genetic Polymorphism in Heterogeneous Environments: A Decade Later
journal, November 1986


Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata : GENETIC BASIS OF LOCAL ADAPTATION IN
journal, June 2012


The Role of Ecotypic Variation in the Distribution of the Central Grassland of North America
journal, February 1959

  • McMillan, Calvin
  • Ecological Monographs, Vol. 29, Issue 4
  • DOI: 10.2307/1942132