Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

VanWallendael, Acer; Bonnette, Jason; Juenger, Thomas E.; Fritschi, Felix B.; Fay, Philip A.; Mitchell, Robert B.; Lloyd‐Reilley, John; Rouquette, Jr., Francis M.; Bergstrom, Gary C.; Lowry, David B.

doi:10.1111/nph.16555

Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

Journal Article · Mon Mar 23 00:00:00 EDT 2020 · New Phytologist

DOI:https://doi.org/10.1111/nph.16555· OSTI ID:1656820

^[1]; ^[2]; ^[2]; ^[3]; ^[4]; Mitchell, Robert B. ^[5]; Lloyd‐Reilley, John ^[6]; ^[7]; ^[8]; ^[9]

Michigan State Univ., East Lansing, MI (United States); USDOE Bioenergy Research Centers (BRC) (United States). Great Lakes Bioenergy Research Center (GLBRC); Michigan State University
Univ. of Texas, Austin, TX (United States)
Univ. of Missouri, Columbia, MO (United States)
USDA‐Agricultural Research Service (ARS) Grassland, Temple, TX (United States)
Univ. of Nebraska Lincoln NE (United States). USDA‐Agricultural Research Service (ARS) Wheat, Sorghum, and Forage Research Unit
USDA‐Natural Resources Conservation Service (NRCS) Kika de la Garza Plant Materials Center, Kingsville, TX (United States)
Texas A&M AgriLife Research and Extension Center Overton, TX (United States)
Cornell Univ., Ithaca, NY (United States)
Michigan State Univ., East Lansing, MI (United States); USDOE Bioenergy Research Centers (BRC) (United States). Great Lakes Bioenergy Research Center (GLBRC)

Local adaptation is an important process in plant evolution, which can be impacted by differential pathogen pressures along environmental gradients. However, the degree to which pathogen resistance loci vary in effect across space and time is incompletely described. As such, to understand how the genetic architecture of resistance varies across time and geographic space, we quantified rust (Puccinia spp.) severity in switchgrass (Panicum virgatum) plantings at eight locations across the central USA for 3 yr and conducted quantitative trait locus (QTL) mapping for rust progression. We mapped several variable QTLs, but two large-effect QTLs which we have named Prr1 and Prr2 were consistently associated with rust severity in multiple sites and years, particularly in northern sites. By contrast, there were numerous small-effect QTLs at southern sites, indicating a genotype-by-environment interaction in rust resistance loci. Interestingly, Prr1 and Prr2 had a strong epistatic interaction, which also varied in the strength and direction of effect across space. Our results suggest that abiotic factors covarying with latitude interact with the genetic loci underlying plant resistance to control rust infection severity. Furthermore, our results indicate that segregating genetic variation in epistatically interacting loci may play a key role in determining response to infection across geographic space.

View Accepted Manuscript (DOE)

Research Organization:: Michigan State Univ., East Lansing, MI (United States); USDOE Bioenergy Research Centers (BRC) (United States). Great Lakes Bioenergy Research Center (GLBRC); Univ. of Texas, Austin, TX (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

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

OSTI ID:: 1656820

Alternate ID(s):: OSTI ID: 1615701
OSTI ID: 1773851

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 6 Vol. 227; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Strain-specific and recessive QTLs involved in the control of partial resistance to Fusarium oxysporum f. sp. melonis race 1.2 in a recombinant inbred line population of melon Perchepied, L.; Dogimont, C.; Pitrat, M. Theoretical and Applied Genetics, Vol. 111, Issue 1 https://doi.org/10.1007/s00122-005-1991-y	journal	April 2005
Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana Tian, D.; Traw, M. B.; Chen, J. Q. Nature, Vol. 423, Issue 6935 https://doi.org/10.1038/nature01588	journal	May 2003
Biological and biomedical implications of the co-evolution of pathogens and their hosts Woolhouse, Mark E. J.; Webster, Joanne P.; Domingo, Esteban Nature Genetics, Vol. 32, Issue 4 https://doi.org/10.1038/ng1202-569	journal	December 2002
Sar Increases Fitness of Arabidopsis Thaliana in the Presence of Natural Bacterial Pathogens Traw, M. Brian; Kniskern, Joel M.; Bergelson, Joy Evolution, Vol. 61, Issue 10 https://doi.org/10.1111/j.1558-5646.2007.00211.x	journal	October 2007
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
Switchgrass and Giant Miscanthus Agronomy Lee, D. K.; Parrish, Allen S.; Voigt, Thomas B. Engineering and Science of Biomass Feedstock Production and Provision https://doi.org/10.1007/978-1-4899-8014-4_3	book	January 2014
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Data Analysis Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4_9	book	June 2016
Stripe rust and leaf rust resistance QTL mapping, epistatic interactions, and co-localization with stem rust resistance loci in spring wheat evaluated over three continents Singh, A.; Knox, R. E.; DePauw, R. M. Theoretical and Applied Genetics, Vol. 127, Issue 11 https://doi.org/10.1007/s00122-014-2390-z	journal	September 2014
Multi-location wheat stripe rust QTL analysis: genetic background and epistatic interactions Vazquez, M. Dolores; Zemetra, Robert; Peterson, C. James Theoretical and Applied Genetics, Vol. 128, Issue 7 https://doi.org/10.1007/s00122-015-2507-z	journal	April 2015
A major QTL co-localized on chromosome 6BL and its epistatic interaction for enhanced wheat stripe rust resistance Zeng, Qingdong; Wu, Jianhui; Liu, Shengjie Theoretical and Applied Genetics, Vol. 132, Issue 5 https://doi.org/10.1007/s00122-019-03288-2	journal	February 2019
The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars Jeger, M. J.; Viljanen-Rollinson, S. L. H. Theoretical and Applied Genetics, Vol. 102, Issue 1 https://doi.org/10.1007/s001220051615	journal	January 2001
New insight into the species diversity and life cycles of rust fungi (Pucciniales) affecting bioenergy switchgrass (Panicum virgatum) in the Eastern and Central United States Kenaley, Shawn C.; Quan, Menchus; Aime, M. Catherine Mycological Progress, Vol. 17, Issue 11 https://doi.org/10.1007/s11557-018-1434-1	journal	October 2018
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
Plant immune system incompatibility and the distribution of enemies in natural hybrid zones Traw, M. Brian; Bergelson, Joy Current Opinion in Plant Biology, Vol. 13, Issue 4 https://doi.org/10.1016/j.pbi.2010.04.009	journal	August 2010
Early Detection of Systemic Rust Infections of Dyers Woad ( Isatis tinctoria ) Using the Polymerase Chain Reaction Kropp, Bradley R.; Albee, Steve; Flint, Karen M. Weed Science, Vol. 43, Issue 3 https://doi.org/10.1017/S0043174500081480	journal	September 1995
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
Climate change patterns in Amazonia and biodiversity Cheng, Hai; Sinha, Ashish; Cruz, Francisco W. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2415	journal	January 2013
Highly confined ions store charge more efficiently in supercapacitors Merlet, C.; Péan, C.; Rotenberg, B. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3701	journal	October 2013
Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species Bomblies, Kirsten; Weigel, Detlef Nature Reviews Genetics, Vol. 8, Issue 5 https://doi.org/10.1038/nrg2082	journal	April 2007
In situ click chemistry generation of cyclooxygenase-2 inhibitors Bhardwaj, Atul; Kaur, Jatinder; Wuest, Melinda Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-016-0009-6	journal	February 2017
Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis Huot, Bethany; Castroverde, Christian Danve M.; Velásquez, André C. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01674-2	journal	November 2017
No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird Koch, Rebecca E.; Kavazis, Andreas N.; Hasselquist, Dennis Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-02974-x	journal	February 2018
Double-slit photoelectron interference in strong-field ionization of the neon dimer Kunitski, Maksim; Eicke, Nicolas; Huber, Pia Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-07882-8	journal	January 2019
SMARCAD1 ATPase activity is required to silence endogenous retroviruses in embryonic stem cells Sachs, Parysatis; Ding, Dong; Bergmaier, Philipp Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09078-0	journal	March 2019
Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits Mckay, J. K.; Richards, J. H.; Mitchell-Olds, T. Molecular Ecology, Vol. 12, Issue 5 https://doi.org/10.1046/j.1365-294X.2003.01833.x	journal	May 2003
Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal Thrall, P. H.; Burdon, J. J. Plant Pathology, Vol. 51, Issue 2 https://doi.org/10.1046/j.1365-3059.2002.00683.x	journal	April 2002
Evolution of host range in Coleosporium ipomoeae , a plant pathogen with multiple hosts Chappell, Thomas M.; Rausher, Mark D. Proceedings of the National Academy of Sciences, Vol. 113, Issue 19 https://doi.org/10.1073/pnas.1522997113	journal	April 2016
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
QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient Lowry, David B.; Lovell, John T.; Zhang, Li Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1821543116	journal	June 2019
Rust fungi on Panicum Demers, Jill E.; Liu, Miao; Hambleton, Sarah Mycologia, Vol. 109, Issue 1 https://doi.org/10.1080/00275514.2016.1262656	journal	January 2017
Epidemiology and control of stripe rust [ Puccinia striiformis f. sp. tritici ] on wheat Chen, X. M. Canadian Journal of Plant Pathology, Vol. 27, Issue 3 https://doi.org/10.1080/07060660509507230	journal	September 2005
An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences Aime, M. Catherine; Matheny, P. Brandon; Henk, Daniel A. Mycologia, Vol. 98, Issue 6 https://doi.org/10.1080/15572536.2006.11832619	journal	November 2006
A Quantitative Survey of Local Adaptation and Fitness Trade‐Offs Hereford, Joe The American Naturalist, Vol. 173, Issue 5 https://doi.org/10.1086/597611	journal	May 2009
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
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
Natural Selection, Infectious Transfer and the Existence Conditions for Bacterial Plasmids Bergstrom, Carl T.; Lipsitch, Marc; Levin, Bruce R. Genetics, Vol. 155, Issue 4 https://doi.org/10.1093/genetics/155.4.1505	journal	August 2000
The interaction of plant biotic and abiotic stresses: from genes to the field Atkinson, N. J.; Urwin, P. E. Journal of Experimental Botany, Vol. 63, Issue 10 https://doi.org/10.1093/jxb/ers100	journal	March 2012
Emergence and Spread of New Races of Wheat Stem Rust Fungus: Continued Threat to Food Security and Prospects of Genetic Control Singh, Ravi P.; Hodson, David P.; Jin, Yue Phytopathology, Vol. 105, Issue 7 https://doi.org/10.1094/PHYTO-01-15-0030-FI	journal	July 2015
Promises and challenges of eco-physiological genomics in the field: tests of drought responses in switchgrass Lovell, John T.; Shakirov, Eugene V.; Schwartz, Scott Plant Physiology https://doi.org/10.1104/pp.16.00545	journal	May 2016
NLR Mutations Suppressing Immune Hybrid Incompatibility and Their Effects on Disease Resistance Atanasov, Kostadin E.; Liu, Changxin; Erban, Alexander Plant Physiology, Vol. 177, Issue 3 https://doi.org/10.1104/pp.18.00462	journal	May 2018
Differentiating genetic and environmental drivers of plant-pathogen community interactions Busby, Posy E.; Newcombe, George; Dirzo, Rodolfo Journal of Ecology, Vol. 102, Issue 5 https://doi.org/10.1111/1365-2745.12270	journal	June 2014
Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection Alexander, Helen M.; Bruns, Emily; Schebor, Hayley Journal of Ecology, Vol. 105, Issue 4 https://doi.org/10.1111/1365-2745.12723	journal	January 2017
Understanding the ecology and evolution of host-parasite interactions across scales Penczykowski, Rachel M.; Laine, Anna-Liisa; Koskella, Britt Evolutionary Applications, Vol. 9, Issue 1 https://doi.org/10.1111/eva.12294	journal	August 2015
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
Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape: GENOMIC DIVERSITY IN SWITCHGRASS Morris, Geoffrey P.; Grabowski, Paul P.; Borevitz, Justin O. Molecular Ecology, Vol. 20, Issue 23 https://doi.org/10.1111/j.1365-294X.2011.05335.x	journal	November 2011
Geographic distribution of plant pathogens in response to climate change: Pathogen distributions and climate Shaw, M. W.; Osborne, T. M. Plant Pathology, Vol. 60, Issue 1 https://doi.org/10.1111/j.1365-3059.2010.02407.x	journal	January 2011
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
Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation: Coevolution in a wild host-pathogen system Thrall, Peter H.; Laine, Anna-Liisa; Ravensdale, Michael Ecology Letters, Vol. 15, Issue 5 https://doi.org/10.1111/j.1461-0248.2012.01749.x	journal	February 2012
Major-gene resistance to the rust pathogen Coleosporium ipomoeae is common in natural populations of Ipomoea purpurea Kniskern, Joel M.; Rausher, Mark D. New Phytologist, Vol. 171, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01729.x	journal	July 2006
Costs and Benefits of Plant Responses to Disease: Resistance and Tolerance Simms, Ellen L.; Triplett, Jim Evolution, Vol. 48, Issue 6 https://doi.org/10.1111/j.1558-5646.1994.tb02227.x	journal	December 1994
Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution Giraud, Tatiana; Koskella, Britt; Laine, Anna-Liisa Molecular Ecology, Vol. 26, Issue 7 https://doi.org/10.1111/mec.14091	journal	April 2017
Spatial variation in soil biota mediates plant adaptation to a foliar pathogen Mursinoff, Sini; Tack, Ayco J. M. New Phytologist, Vol. 214, Issue 2 https://doi.org/10.1111/nph.14402	journal	January 2017
A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust Fu, D.; Uauy, C.; Distelfeld, A. Science, Vol. 323, Issue 5919 https://doi.org/10.1126/science.1166289	journal	March 2009
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
When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Hybrid Incompatibilities Fishman, Lila; Sweigart, Andrea L. Annual Review of Plant Biology, Vol. 69, Issue 1 https://doi.org/10.1146/annurev-arplant-042817-040113	journal	April 2018
Maintenance of Plant Species Diversity by Pathogens Bever, James D.; Mangan, Scott A.; Alexander, Helen M. Annual Review of Ecology, Evolution, and Systematics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-ecolsys-112414-054306	journal	December 2015
Effects of Environmental Factors on Plant Disease Colhoun, J. Annual Review of Phytopathology, Vol. 11, Issue 1 https://doi.org/10.1146/annurev.py.11.090173.002015	journal	September 1973
Development of a New USDA Plant Hardiness Zone Map for the United States Daly, Christopher; Widrlechner, Mark P.; Halbleib, Michael D. Journal of Applied Meteorology and Climatology, Vol. 51, Issue 2 https://doi.org/10.1175/2010JAMC2536.1	journal	February 2012
A Meta-Analysis of Local Adaptation in Plants Leimu, Roosa; Fischer, Markus PLoS ONE, Vol. 3, Issue 12 https://doi.org/10.1371/journal.pone.0004010	journal	December 2008
Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen Puccinia striiformis f.sp. tritici Ali, Sajid; Gladieux, Pierre; Leconte, Marc PLoS Pathogens, Vol. 10, Issue 1 https://doi.org/10.1371/journal.ppat.1003903	journal	January 2014
Mapping Quantitative Trait Loci Underlying Function-Valued Traits Using Functional Principal Component Analysis and Multi-Trait Mapping Kwak, Il-Youp; Moore, Candace R.; Spalding, Edgar P. G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 1 https://doi.org/10.1534/g3.115.024133	journal	November 2015
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
A Simple Regression-Based Method to Map Quantitative Trait Loci Underlying Function-Valued Phenotypes Kwak, Il-Youp; Moore, Candace R.; Spalding, Edgar P. Genetics, Vol. 197, Issue 4 https://doi.org/10.1534/genetics.114.166306	journal	June 2014
Costs and Benefits of Plant Responses to Disease: Resistance and Tolerance Simms, Ellen L.; Triplett, Jim Evolution, Vol. 48, Issue 6 https://doi.org/10.2307/2410521	journal	December 1994
RNAi-Mediated Downregulation of Inositol Pentakisphosphate Kinase (IPK1) in Wheat Grains Decreases Phytic Acid Levels and Increases Fe and Zn Accumulation Aggarwal, Sipla; Kumar, Anil; Bhati, Kaushal K. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00259	journal	March 2018
Genetic Analysis of Flooding Tolerance in an Andean Diversity Panel of Dry Bean (Phaseolus vulgaris L.) Soltani, Ali; MafiMoghaddam, Samira; Oladzad-Abbasabadi, Atena Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00767	journal	June 2018
Climate vs. soil Factors in Local Adaptation of two Common Plant Species Macel, Mirka; Lawson, Clare S.; Mortimer, Simon R. Figshare https://doi.org/10.6084/m9.figshare.c.3299591	collection	January 2016

Similar Records

The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass (Panicum virgatum)

Journal Article · Thu Sep 08 20:00:00 EDT 2016 · G3 · OSTI ID:1423766

Related Subjects

09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
GxE
Puccinia
QTL mapping
local adaptation
pathogen QTL switchgrass
pathogen resistance
switchgrass (Panicum virgatum)

Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

Citation Formats

References (68)

Similar Records

Related Subjects