Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)
Abstract
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. 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.
- Authors:
-
[1];
[2];
[2];
[3];
[4];
[7];
[8];
[1]
- 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)
- 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)
- Publication Date:
- Research Org.:
- 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 Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1656820
- Alternate Identifier(s):
- OSTI ID: 1615701; OSTI ID: 1773851
- Grant/Contract Number:
- SC0017883; SC0014156; IOS-0922457; IOS-1444533; SC0018409; FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 227; Journal Issue: 6; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; GxE; local adaptation; pathogen resistance; Puccinia; QTL mapping; switchgrass (Panicum virgatum); pathogen QTL switchgrass
Citation Formats
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., and Lowry, David B. Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum). United States: N. p., 2020.
Web. doi:10.1111/nph.16555.
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. Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum). United States. https://doi.org/10.1111/nph.16555
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., and Lowry, David B. Mon .
"Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)". United States. https://doi.org/10.1111/nph.16555. https://www.osti.gov/servlets/purl/1656820.
@article{osti_1656820,
title = {Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)},
author = {VanWallendael, Acer and Bonnette, Jason and Juenger, Thomas E. and Fritschi, Felix B. and Fay, Philip A. and Mitchell, Robert B. and Lloyd‐Reilley, John and Rouquette, Jr., Francis M. and Bergstrom, Gary C. and Lowry, David B.},
abstractNote = {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. 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.},
doi = {10.1111/nph.16555},
journal = {New Phytologist},
number = 6,
volume = 227,
place = {United States},
year = {2020},
month = {3}
}
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Works referenced in this record:
Double-slit photoelectron interference in strong-field ionization of the neon dimer
journal, January 2019
- Kunitski, Maksim; Eicke, Nicolas; Huber, Pia
- Nature Communications, Vol. 10, Issue 1
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
Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen Puccinia striiformis f.sp. tritici
journal, January 2014
- Ali, Sajid; Gladieux, Pierre; Leconte, Marc
- PLoS Pathogens, Vol. 10, Issue 1
Differentiating genetic and environmental drivers of plant-pathogen community interactions
journal, June 2014
- Busby, Posy E.; Newcombe, George; Dirzo, Rodolfo
- Journal of Ecology, Vol. 102, Issue 5
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
The interaction of plant biotic and abiotic stresses: from genes to the field
journal, March 2012
- Atkinson, N. J.; Urwin, P. E.
- Journal of Experimental Botany, Vol. 63, Issue 10
Promises and challenges of eco-physiological genomics in the field: tests of drought responses in switchgrass
journal, May 2016
- Lovell, John T.; Shakirov, Eugene V.; Schwartz, Scott
- Plant Physiology
Early Detection of Systemic Rust Infections of Dyers Woad ( Isatis tinctoria ) Using the Polymerase Chain Reaction
journal, September 1995
- Kropp, Bradley R.; Albee, Steve; Flint, Karen M.
- Weed Science, Vol. 43, Issue 3
Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis
journal, November 2017
- Huot, Bethany; Castroverde, Christian Danve M.; Velásquez, André C.
- Nature Communications, Vol. 8, Issue 1
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
A major QTL co-localized on chromosome 6BL and its epistatic interaction for enhanced wheat stripe rust resistance
journal, February 2019
- Zeng, Qingdong; Wu, Jianhui; Liu, Shengjie
- Theoretical and Applied Genetics, Vol. 132, Issue 5
SMARCAD1 ATPase activity is required to silence endogenous retroviruses in embryonic stem cells
journal, March 2019
- Sachs, Parysatis; Ding, Dong; Bergmaier, Philipp
- Nature Communications, Vol. 10, Issue 1
Plant immune system incompatibility and the distribution of enemies in natural hybrid zones
journal, August 2010
- Traw, M. Brian; Bergelson, Joy
- Current Opinion in Plant Biology, Vol. 13, Issue 4
A Quantitative Survey of Local Adaptation and Fitness Trade‐Offs
journal, May 2009
- Hereford, Joe
- The American Naturalist, Vol. 173, Issue 5
Major-gene resistance to the rust pathogen Coleosporium ipomoeae is common in natural populations of Ipomoea purpurea
journal, July 2006
- Kniskern, Joel M.; Rausher, Mark D.
- New Phytologist, Vol. 171, Issue 1
Understanding the ecology and evolution of host-parasite interactions across scales
journal, August 2015
- Penczykowski, Rachel M.; Laine, Anna-Liisa; Koskella, Britt
- Evolutionary Applications, Vol. 9, Issue 1
Development of a New USDA Plant Hardiness Zone Map for the United States
journal, February 2012
- Daly, Christopher; Widrlechner, Mark P.; Halbleib, Michael D.
- Journal of Applied Meteorology and Climatology, Vol. 51, Issue 2
Rust fungi on Panicum
journal, January 2017
- Demers, Jill E.; Liu, Miao; Hambleton, Sarah
- Mycologia, Vol. 109, Issue 1
R/qtl: QTL mapping in experimental crosses
journal, May 2003
- Broman, K. W.; Wu, H.; Sen, S.
- Bioinformatics, Vol. 19, Issue 7
QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient
journal, June 2019
- Lowry, David B.; Lovell, John T.; Zhang, Li
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 26
Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape: GENOMIC DIVERSITY IN SWITCHGRASS
journal, November 2011
- Morris, Geoffrey P.; Grabowski, Paul P.; Borevitz, Justin O.
- Molecular Ecology, Vol. 20, Issue 23
Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection
journal, January 2017
- Alexander, Helen M.; Bruns, Emily; Schebor, Hayley
- Journal of Ecology, Vol. 105, Issue 4
NLR Mutations Suppressing Immune Hybrid Incompatibility and Their Effects on Disease Resistance
journal, May 2018
- Atanasov, Kostadin E.; Liu, Changxin; Erban, Alexander
- Plant Physiology, Vol. 177, Issue 3
Geographic distribution of plant pathogens in response to climate change: Pathogen distributions and climate
journal, January 2011
- Shaw, M. W.; Osborne, T. M.
- Plant Pathology, Vol. 60, Issue 1
Highly confined ions store charge more efficiently in supercapacitors
journal, October 2013
- Merlet, C.; Péan, C.; Rotenberg, B.
- Nature Communications, Vol. 4, Issue 1
Spatial variation in soil biota mediates plant adaptation to a foliar pathogen
journal, January 2017
- Mursinoff, Sini; Tack, Ayco J. M.
- New Phytologist, Vol. 214, Issue 2
Climate change patterns in Amazonia and biodiversity
journal, January 2013
- Cheng, Hai; Sinha, Ashish; Cruz, Francisco W.
- Nature Communications, Vol. 4, Issue 1
In situ click chemistry generation of cyclooxygenase-2 inhibitors
journal, February 2017
- Bhardwaj, Atul; Kaur, Jatinder; Wuest, Melinda
- Nature Communications, Vol. 8, Issue 1
Mapping Quantitative Trait Loci Underlying Function-Valued Traits Using Functional Principal Component Analysis and Multi-Trait Mapping
journal, November 2015
- Kwak, Il-Youp; Moore, Candace R.; Spalding, Edgar P.
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 1
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
journal, September 2014
- Singh, A.; Knox, R. E.; DePauw, R. M.
- Theoretical and Applied Genetics, Vol. 127, Issue 11
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
Evolution of host range in Coleosporium ipomoeae , a plant pathogen with multiple hosts
journal, April 2016
- Chappell, Thomas M.; Rausher, Mark D.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 19
Conceptual issues in local adaptation
journal, December 2004
- Kawecki, Tadeusz J.; Ebert, Dieter
- Ecology Letters, Vol. 7, Issue 12
RNAi-Mediated Downregulation of Inositol Pentakisphosphate Kinase (IPK1) in Wheat Grains Decreases Phytic Acid Levels and Increases Fe and Zn Accumulation
journal, March 2018
- Aggarwal, Sipla; Kumar, Anil; Bhati, Kaushal K.
- Frontiers in Plant Science, Vol. 9
Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation: Coevolution in a wild host-pathogen system
journal, February 2012
- Thrall, Peter H.; Laine, Anna-Liisa; Ravensdale, Michael
- Ecology Letters, Vol. 15, Issue 5
Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits
journal, May 2003
- Mckay, J. K.; Richards, J. H.; Mitchell-Olds, T.
- Molecular Ecology, Vol. 12, Issue 5
A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust
journal, March 2009
- Fu, D.; Uauy, C.; Distelfeld, A.
- Science, Vol. 323, Issue 5919
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
Costs and Benefits of Plant Responses to Disease: Resistance and Tolerance
journal, December 1994
- Simms, Ellen L.; Triplett, Jim
- Evolution, Vol. 48, Issue 6
Epidemiology and control of stripe rust [ Puccinia striiformis f. sp. tritici ] on wheat
journal, September 2005
- Chen, X. M.
- Canadian Journal of Plant Pathology, Vol. 27, Issue 3
Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species
journal, April 2007
- Bomblies, Kirsten; Weigel, Detlef
- Nature Reviews Genetics, Vol. 8, Issue 5
Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal
journal, April 2002
- Thrall, P. H.; Burdon, J. J.
- Plant Pathology, Vol. 51, Issue 2
Genetic Analysis of Flooding Tolerance in an Andean Diversity Panel of Dry Bean (Phaseolus vulgaris L.)
journal, June 2018
- Soltani, Ali; MafiMoghaddam, Samira; Oladzad-Abbasabadi, Atena
- Frontiers in Plant Science, Vol. 9
No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird
journal, February 2018
- Koch, Rebecca E.; Kavazis, Andreas N.; Hasselquist, Dennis
- Nature Communications, Vol. 9, Issue 1
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
journal, October 2018
- Kenaley, Shawn C.; Quan, Menchus; Aime, M. Catherine
- Mycological Progress, Vol. 17, Issue 11
Maintenance of Plant Species Diversity by Pathogens
journal, December 2015
- Bever, James D.; Mangan, Scott A.; Alexander, Helen M.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 46, Issue 1
Multi-location wheat stripe rust QTL analysis: genetic background and epistatic interactions
journal, April 2015
- Vazquez, M. Dolores; Zemetra, Robert; Peterson, C. James
- Theoretical and Applied Genetics, Vol. 128, Issue 7
Effects of Environmental Factors on Plant Disease
journal, September 1973
- Colhoun, J.
- Annual Review of Phytopathology, Vol. 11, Issue 1
A Map of Local Adaptation in Arabidopsis thaliana
journal, October 2011
- Fournier-Level, A.; Korte, A.; Cooper, M. D.
- Science, Vol. 334, Issue 6052
The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars
journal, January 2001
- Jeger, M. J.; Viljanen-Rollinson, S. L. H.
- Theoretical and Applied Genetics, Vol. 102, Issue 1
When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Hybrid Incompatibilities
journal, April 2018
- Fishman, Lila; Sweigart, Andrea L.
- Annual Review of Plant Biology, Vol. 69, Issue 1
Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution
journal, April 2017
- Giraud, Tatiana; Koskella, Britt; Laine, Anna-Liisa
- Molecular Ecology, Vol. 26, Issue 7
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
A Simple Regression-Based Method to Map Quantitative Trait Loci Underlying Function-Valued Phenotypes
journal, June 2014
- Kwak, Il-Youp; Moore, Candace R.; Spalding, Edgar P.
- Genetics, Vol. 197, Issue 4
Emergence and Spread of New Races of Wheat Stem Rust Fungus: Continued Threat to Food Security and Prospects of Genetic Control
journal, July 2015
- Singh, Ravi P.; Hodson, David P.; Jin, Yue
- Phytopathology, Vol. 105, Issue 7
An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences
journal, November 2006
- Aime, M. Catherine; Matheny, P. Brandon; Henk, Daniel A.
- Mycologia, Vol. 98, Issue 6
Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana
journal, May 2003
- Tian, D.; Traw, M. B.; Chen, J. Q.
- Nature, Vol. 423, Issue 6935
A Meta-Analysis of Local Adaptation in Plants
journal, December 2008
- Leimu, Roosa; Fischer, Markus
- PLoS ONE, Vol. 3, Issue 12
Natural Selection, Infectious Transfer and the Existence Conditions for Bacterial Plasmids
journal, August 2000
- Bergstrom, Carl T.; Lipsitch, Marc; Levin, Bruce R.
- Genetics, Vol. 155, Issue 4
Costs and Benefits of Plant Responses to Disease: Resistance and Tolerance
journal, December 1994
- Simms, Ellen L.; Triplett, Jim
- Evolution, Vol. 48, Issue 6