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

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.

doi:10.1073/pnas.1821543116

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

Journal Article · Mon Jun 10 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1821543116· OSTI ID:1525532

; 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;

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.

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Research Organization:: 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 Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation Plant Genome Research Program Award

Contributing Organization:: Only Michigan State University received funding directly by this grant for this publication.

Grant/Contract Number:: AC02-05CH11231; SC0014156; SC0017883; SC0018409; FC02-07ER64494

OSTI ID:: 1525532

Alternate ID(s):: OSTI ID: 1572023; OSTI ID: 1593753

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 116 Journal Issue: 26; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 53 works

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References (56)

Characterization of the Rust Fungus, Puccinia emaculata, and Evaluation of Genetic Variability for Rust Resistance in Switchgrass Populations Uppalapati, Srinivasa Rao; Serba, Desalegn D.; Ishiga, Yasuhiro BioEnergy Research, Vol. 6, Issue 2 https://doi.org/10.1007/s12155-012-9263-6	journal	October 2012
Bmp4 and Morphological Variation of Beaks in Darwin's Finches Abzhanov, A. Science, Vol. 305, Issue 5689 https://doi.org/10.1126/science.1098095	journal	September 2004
The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass ( Panicum virgatum) Milano, Elizabeth R.; Lowry, David B.; Juenger, Thomas E. G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 11 https://doi.org/10.1534/g3.116.032763	journal	September 2016
Identifying loci under selection across contrasting environments in Avena barbata using quantitative trait locus mapping: QTL FOR FITNESS IN AVENA Gardner, Kyle M.; Latta, Robert G. Molecular Ecology, Vol. 15, Issue 5 https://doi.org/10.1111/j.1365-294X.2005.02835.x	journal	January 2006
The statistical analysis of multi-environment data: modeling genotype-by-environment interaction and its genetic basis Malosetti, Marcos; Ribaut, Jean-Marcel; van Eeuwijk, Fred A. Frontiers in Physiology, Vol. 4 https://doi.org/10.3389/fphys.2013.00044	journal	January 2013
Extensive Genetic Diversity is Present within North American Switchgrass Germplasm Evans, Joseph; Sanciangco, Millicent D.; Lau, Kin H. The Plant Genome, Vol. 11, Issue 1 https://doi.org/10.3835/plantgenome2017.06.0055	journal	January 2018
Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix Li, J.; Ji, L. Heredity, Vol. 95, Issue 3 https://doi.org/10.1038/sj.hdy.6800717	journal	August 2005
Linking a mutation to survival in wild mice Barrett, Rowan D. H.; Laurent, Stefan; Mallarino, Ricardo Science, Vol. 363, Issue 6426 https://doi.org/10.1126/science.aav3824	journal	January 2019
Evidence for Ecological Speciation and Its Alternative Schluter, D. Science, Vol. 323, Issue 5915 https://doi.org/10.1126/science.1160006	journal	February 2009
Best Linear Unbiased Estimation and Prediction under a Selection Model Henderson, C. R. Biometrics, Vol. 31, Issue 2 https://doi.org/10.2307/2529430	journal	June 1975
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Improved experimental protocols to evaluate cold tolerance thresholds in Miscanthus and switchgrass rhizomes Peixoto, Murilo de Melo; Sage, Rowan F. GCB Bioenergy, Vol. 8, Issue 2 https://doi.org/10.1111/gcbb.12301	journal	January 2016
Switchgrass Breeding, Genetics, and Genomics Casler, Michael D. Green Energy and Technology (book series) https://doi.org/10.1007/978-1-4471-2903-5_2	book	January 2012
Latitudinal and Longitudinal Adaptation of Switchgrass Populations Casler, M. D.; Vogel, K. P.; Taliaferro, C. M. Crop Science, Vol. 47, Issue 6 https://doi.org/10.2135/cropsci2006.12.0780	journal	January 2007
Latitudinal Adaptation of Switchgrass Populations Casler, M. D.; Vogel, K. P.; Taliaferro, C. M. Crop Science, Vol. 44, Issue 1 https://doi.org/10.2135/cropsci2004.2930	journal	January 2004
An Overview of the Global Historical Climatology Network-Daily Database Menne, Matthew J.; Durre, Imke; Vose, Russell S. Journal of Atmospheric and Oceanic Technology, Vol. 29, Issue 7 https://doi.org/10.1175/JTECH-D-11-00103.1	journal	July 2012
Perennial Biomass Grasses and the Mason–Dixon Line: Comparative Productivity across Latitudes in the Southern Great Plains Kiniry, J. R.; Anderson, L. C.; Johnson, M. -V. V. BioEnergy Research, Vol. 6, Issue 1 https://doi.org/10.1007/s12155-012-9254-7	journal	September 2012
Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range Ågren, Jon; Schemske, Douglas W. New Phytologist, Vol. 194, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04112.x	journal	March 2012
Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana Agren, J.; Oakley, C. G.; McKay, J. K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 52 https://doi.org/10.1073/pnas.1316773110	journal	December 2013
R/qtl: QTL mapping in experimental crosses Broman, K. W.; Wu, H.; Sen, S. Bioinformatics, Vol. 19, Issue 7 https://doi.org/10.1093/bioinformatics/btg112	journal	May 2003
A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern Hoekstra, Hopi E.; Hirschmann, Rachel J.; Bundey, Richard A. Science, Vol. 313, Issue 5783 https://doi.org/10.1126/science.1126121	journal	July 2006
Modern Applied Statistics with S Venables, W. N.; Ripley, B. D. Statistics and Computing https://doi.org/10.1007/978-0-387-21706-2	book	August 2002
Polyploidy and Winter Survival in Panicum virgatum L.1 Nielsen, Etlar L. Agronomy Journal, Vol. 39, Issue 9 https://doi.org/10.2134/agronj1947.00021962003900090010x	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 Aspinwall, Michael J.; Lowry, David B.; Taylor, Samuel H. New Phytologist, Vol. 199, Issue 4 https://doi.org/10.1111/nph.12341	journal	May 2013
Ecological genomics of local adaptation Savolainen, Outi; Lascoux, Martin; Merilä, Juha Nature Reviews Genetics, Vol. 14, Issue 11 https://doi.org/10.1038/nrg3522	journal	October 2013
Population genomic variation reveals roles of history, adaptation and ploidy in switchgrass Grabowski, Paul P.; Morris, Geoffrey P.; Casler, Michael D. Molecular Ecology, Vol. 23, Issue 16 https://doi.org/10.1111/mec.12845	journal	July 2014
Switchgrass Germplasm Resources Casler, Michael D.; Vogel, Kenneth P.; Harrison, Melanie Crop Science, Vol. 55, Issue 6 https://doi.org/10.2135/cropsci2015.02.0076	journal	January 2015
VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing Koboldt, D. C.; Zhang, Q.; Larson, D. E. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.129684.111	journal	February 2012
Reduction of Ethanol Yield from Switchgrass Infected with Rust Caused by Puccinia emaculata Sykes, Virginia R.; Allen, Fred L.; Mielenz, Jonathan R. BioEnergy Research, Vol. 9, Issue 1 https://doi.org/10.1007/s12155-015-9680-4	journal	October 2015
Conceptual issues in local adaptation Kawecki, Tadeusz J.; Ebert, Dieter Ecology Letters, Vol. 7, Issue 12 https://doi.org/10.1111/j.1461-0248.2004.00684.x	journal	December 2004
Conducting Meta-Analyses in R with the metafor Package Viechtbauer, Wolfgang Journal of Statistical Software, Vol. 36, Issue 3 https://doi.org/10.18637/jss.v036.i03	journal	January 2010
Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Lander, E. S.; Botstein, D. Genetics, Vol. 121, Issue 1 https://doi.org/10.1093/genetics/121.1.185	journal	January 1989
Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation Wadgymar, Susana M.; Lowry, David B.; Gould, Billie A. Methods in Ecology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1111/2041-210X.12777	journal	June 2017
Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum Lowry, David B.; Behrman, Kathrine D.; Grabowski, Paul The American Naturalist, Vol. 183, Issue 5 https://doi.org/10.1086/675760	journal	May 2014
A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation Lowry, David B.; Willis, John H. PLoS Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pbio.1000500	journal	September 2010
bnstruct: an R package for Bayesian Network structure learning in the presence of missing data Franzin, Alberto; Sambo, Francesco; Di Camillo, Barbara Bioinformatics, Vol. 33, Issue 8 https://doi.org/10.1093/bioinformatics/btw807	journal	December 2016
Genomics of local adaptation with gene flow Tigano, Anna; Friesen, Vicki L. Molecular Ecology, Vol. 25, Issue 10 https://doi.org/10.1111/mec.13606	journal	April 2016
Testing for local adaptation in Avena barbata : a classic example of ecotypic divergence Latta, Robert G. Molecular Ecology, Vol. 18, Issue 18 https://doi.org/10.1111/j.1365-294X.2009.04302.x	journal	September 2009
C ₄ bioenergy crops for cool climates, with special emphasis on perennial C ₄ grasses Sage, Rowan F.; de Melo Peixoto, Murilo; Friesen, Patrick Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv123	journal	April 2015
Plant Mortality and Natural Selection May Increase Biomass Yield in Switchgrass Swards Casler, Michael D.; Smart, Alexander J. Crop Science, Vol. 53, Issue 2 https://doi.org/10.2135/cropsci2012.07.0434	journal	January 2013
Ecological speciation: Ecological speciation Rundle, Howard D.; Nosil, Patrik Ecology Letters, Vol. 8, Issue 3 https://doi.org/10.1111/j.1461-0248.2004.00715.x	journal	January 2005
An Analysis of Variation Between Upland and Lowland Switchgrass, Panicum Virgatum L., in Central Oklahoma Porter, Clyde L. Ecology, Vol. 47, Issue 6 https://doi.org/10.2307/1935646	journal	November 1966
TSPmap, a tool making use of traveling salesperson problem solvers in the efficient and accurate construction of high-density genetic linkage maps Monroe, J. Grey; Allen, Zachariah A.; Tanger, Paul BioData Mining, Vol. 10, Issue 1 https://doi.org/10.1186/s13040-017-0158-0	journal	December 2017
Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers Bradshaw, H. D.; Schemske, Douglas W. Nature, Vol. 426, Issue 6963 https://doi.org/10.1038/nature02106	journal	November 2003
A Map of Local Adaptation in Arabidopsis thaliana Fournier-Level, A.; Korte, A.; Cooper, M. D. Science, Vol. 334, Issue 6052 https://doi.org/10.1126/science.1209271	journal	October 2011
The Theoretical Population Genetics of Variable Selection and Migration Felsenstein, J. Annual Review of Genetics, Vol. 10, Issue 1 https://doi.org/10.1146/annurev.ge.10.120176.001345	journal	December 1976
Genetic trade-offs and conditional neutrality contribute to local adaptation: GENETIC BASIS OF LOCAL ADAPTATION Anderson, Jill T.; Lee, Cheng-Ruei; Rushworth, Catherine A. Molecular Ecology, Vol. 22, Issue 3 https://doi.org/10.1111/j.1365-294X.2012.05522.x	journal	March 2012
Genetic Equilibrium When More Than One Ecological Niche is Available Levene, Howard The American Naturalist, Vol. 87, Issue 836 https://doi.org/10.1086/281792	journal	September 1953
Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana Price, Nicholas; Moyers, Brook T.; Lopez, Lua Proceedings of the National Academy of Sciences, Vol. 115, Issue 19 https://doi.org/10.1073/pnas.1719998115	journal	April 2018
Genome-Assisted Prediction of Quantitative Traits Using the R Package sommer Covarrubias-Pazaran, Giovanny PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156744	journal	June 2016
Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data Grabowski, Paul P.; Evans, Joseph; Daum, Chris New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14101	journal	July 2016
Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci?: TRADE-OFFS CAN CONTRIBUTE TO ADAPTATION IN MIMULUS Hall, M. C.; Lowry, D. B.; Willis, J. H. Molecular Ecology, Vol. 19, Issue 13 https://doi.org/10.1111/j.1365-294X.2010.04680.x	journal	June 2010
Genetic Polymorphism in Heterogeneous Environments: A Decade Later Hedrick, P. W. Annual Review of Ecology and Systematics, Vol. 17, Issue 1 https://doi.org/10.1146/annurev.es.17.110186.002535	journal	November 1986
Relative Performance of Non-Local Cultivars and Local, Wild Populations of Switchgrass (Panicum virgatum) in Competition Experiments Palik, D. J.; Snow, A. A.; Stottlemyer, A. L. PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0154444	journal	April 2016
Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata : GENETIC BASIS OF LOCAL ADAPTATION IN Leinonen, PÄIvi H.; Remington, David L.; LeppÄLÄ, Johanna Molecular Ecology, Vol. 22, Issue 3 https://doi.org/10.1111/j.1365-294X.2012.05678.x	journal	June 2012
The Role of Ecotypic Variation in the Distribution of the Central Grassland of North America McMillan, Calvin Ecological Monographs, Vol. 29, Issue 4 https://doi.org/10.2307/1942132	journal	February 1959

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