Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree

Wellington Muchero; Kelsey L. Sondreli; Jin Gui Chen; Breeanna R. Urbanowicz; Jin Zhang; Vasanth Singan; Yongil Yang; Robert S. Brueggeman; Juan Franco-Coronado; Nivi Abraham; Jeong Yeh Yang; Kelley W. Moremen; Alexandra J. Weisberg; Jeff H. Chang; Erika Lindquist; Kerrie Barry; Priya Ranjan; Sara Jawdy; Jeremy Schmutz; Gerald A. Tuskan; Jared M. LeBoldus

doi:10.1073/pnas.1804428115

Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree

Wellington Muchero, Kelsey L. Sondreli, Jin Gui Chen, Breeanna R. Urbanowicz, Jin Zhang, Vasanth Singan, Yongil Yang, Robert S. Brueggeman, Juan Franco-Coronado, Nivi Abraham, Jeong Yeh Yang, Kelley W. Moremen, Alexandra J. Weisberg, Jeff H. Chang, Erika Lindquist, Kerrie Barry, Priya Ranjan, Sara Jawdy, Jeremy Schmutz, Gerald A. TuskanJared M. LeBoldus

Research output: Contribution to journal › Article › peer-review

64 Scopus citations

Abstract

Invasive microbes causing diseases such as sudden oak death negatively affect ecosystems and economies around the world. The deployment of resistant genotypes for combating introduced diseases typically relies on breeding programs that can take decades to complete. To demonstrate how this process can be accelerated, we employed a genome-wide association mapping of ca. 1,000 resequenced Populus trichocarpa trees individually challenged with Sphaerulina musiva, an invasive fungal pathogen. Among significant associations, three loci associated with resistancewere identified and predicted to encode one putative membrane-bound L-type receptorlike kinase and two receptor-like proteins. A susceptibility-associated locus was predicted to encode a putative G-type D-mannose-binding receptor-like kinase. Multiple lines of evidence, including allele analysis, transcriptomics, binding assays, and overexpression, support the hypothesized function of these candidate genes in the P. trichocarpa response to S. musiva.

Original language	English
Pages (from-to)	11573-11578
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	115
Issue number	45
DOIs	https://doi.org/10.1073/pnas.1804428115
State	Published - Nov 6 2018

Funding

ACKNOWLEDGMENTS. This study was supported by Department of Energy (DOE) Office of Science, Office of Biological and Environmental Research (BER) Grant DE-SC0018196, US Department of Agriculture Grant 2012-34103-19771 (to J.M.L.), the Plant–Microbe Interfaces Scientific Focus Area in the DOE BER Genomic Science Program, and the DOE Center for Bioenergy Innovation Project. The Center for Bioenergy Innovation is a US DOE Bioenergy Research Center supported by the Office of BER in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the US DOE under Contract DE-AC05-00OR22725. The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US DOE under Contract DE-AC02-05CH11231. This work was also supported by National Institute of Food and Agriculture, US Department of Agriculture Award 2014-51181-22384 (to J.H.C.). J.-Y.Y. and K.W.M. were supported by NIH Grants P41GM103390 and P01GM107012. We would also like to acknowledge the DOE funded Center for Plant and Microbial Complex Carbohydrates Grant DE-SC0015662 (DE-FG02-93ER20097) for equipment support. This research used resources of the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory.

Funders	Funder number
DOE Center for Bioenergy Innovation Project
DOE Office of Science
DOE funded Center for Plant and Microbial Complex Carbohydrates	DE-FG02-93ER20097, DE-SC0015662
Office of BER
Office of Biological and Environmental Research
DOE Office of Science	DE-AC02-05CH11231
US Department of Agriculture	2012-34103-19771
National Institutes of Health	P41GM103390
U.S. Department of Energy
National Institute of General Medical Sciences	P01GM107012
National Institute of Food and Agriculture	2014-51181-22384
Office of Science
Biological and Environmental Research	DE-SC0018196
Oak Ridge National Laboratory	DE-AC05-00OR22725

Keywords

Association mapping
Disease resistance
Invasive disease
Populus trichocarpa
Septoria canker

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10.1073/pnas.1804428115

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Muchero, W., Sondreli, K. L., Chen, J. G., Urbanowicz, B. R., Zhang, J., Singan, V., Yang, Y., Brueggeman, R. S., Franco-Coronado, J., Abraham, N., Yang, J. Y., Moremen, K. W., Weisberg, A. J., Chang, J. H., Lindquist, E., Barry, K., Ranjan, P., Jawdy, S., Schmutz, J., ... LeBoldus, J. M. (2018). Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree. Proceedings of the National Academy of Sciences of the United States of America, 115(45), 11573-11578. https://doi.org/10.1073/pnas.1804428115

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title = "Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree",

abstract = "Invasive microbes causing diseases such as sudden oak death negatively affect ecosystems and economies around the world. The deployment of resistant genotypes for combating introduced diseases typically relies on breeding programs that can take decades to complete. To demonstrate how this process can be accelerated, we employed a genome-wide association mapping of ca. 1,000 resequenced Populus trichocarpa trees individually challenged with Sphaerulina musiva, an invasive fungal pathogen. Among significant associations, three loci associated with resistancewere identified and predicted to encode one putative membrane-bound L-type receptorlike kinase and two receptor-like proteins. A susceptibility-associated locus was predicted to encode a putative G-type D-mannose-binding receptor-like kinase. Multiple lines of evidence, including allele analysis, transcriptomics, binding assays, and overexpression, support the hypothesized function of these candidate genes in the P. trichocarpa response to S. musiva.",

keywords = "Association mapping, Disease resistance, Invasive disease, Populus trichocarpa, Septoria canker",

author = "Wellington Muchero and Sondreli, {Kelsey L.} and Chen, {Jin Gui} and Urbanowicz, {Breeanna R.} and Jin Zhang and Vasanth Singan and Yongil Yang and Brueggeman, {Robert S.} and Juan Franco-Coronado and Nivi Abraham and Yang, {Jeong Yeh} and Moremen, {Kelley W.} and Weisberg, {Alexandra J.} and Chang, {Jeff H.} and Erika Lindquist and Kerrie Barry and Priya Ranjan and Sara Jawdy and Jeremy Schmutz and Tuskan, {Gerald A.} and LeBoldus, {Jared M.}",

year = "2018",

month = nov,

day = "6",

doi = "10.1073/pnas.1804428115",

language = "English",

volume = "115",

pages = "11573--11578",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Muchero, W, Sondreli, KL, Chen, JG, Urbanowicz, BR, Zhang, J, Singan, V, Yang, Y, Brueggeman, RS, Franco-Coronado, J, Abraham, N, Yang, JY, Moremen, KW, Weisberg, AJ, Chang, JH, Lindquist, E, Barry, K, Ranjan, P , Jawdy, S, Schmutz, J, Tuskan, GA & LeBoldus, JM 2018, 'Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 45, pp. 11573-11578. https://doi.org/10.1073/pnas.1804428115

Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree. / Muchero, Wellington; Sondreli, Kelsey L.; Chen, Jin Gui et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 45, 06.11.2018, p. 11573-11578.

Research output: Contribution to journal › Article › peer-review

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AU - Muchero, Wellington

AU - Sondreli, Kelsey L.

AU - Chen, Jin Gui

AU - Urbanowicz, Breeanna R.

AU - Zhang, Jin

AU - Singan, Vasanth

AU - Yang, Yongil

AU - Brueggeman, Robert S.

AU - Franco-Coronado, Juan

AU - Abraham, Nivi

AU - Yang, Jeong Yeh

AU - Moremen, Kelley W.

AU - Weisberg, Alexandra J.

AU - Chang, Jeff H.

AU - Lindquist, Erika

AU - Barry, Kerrie

AU - Ranjan, Priya

AU - Jawdy, Sara

AU - Schmutz, Jeremy

AU - Tuskan, Gerald A.

AU - LeBoldus, Jared M.

PY - 2018/11/6

Y1 - 2018/11/6

N2 - Invasive microbes causing diseases such as sudden oak death negatively affect ecosystems and economies around the world. The deployment of resistant genotypes for combating introduced diseases typically relies on breeding programs that can take decades to complete. To demonstrate how this process can be accelerated, we employed a genome-wide association mapping of ca. 1,000 resequenced Populus trichocarpa trees individually challenged with Sphaerulina musiva, an invasive fungal pathogen. Among significant associations, three loci associated with resistancewere identified and predicted to encode one putative membrane-bound L-type receptorlike kinase and two receptor-like proteins. A susceptibility-associated locus was predicted to encode a putative G-type D-mannose-binding receptor-like kinase. Multiple lines of evidence, including allele analysis, transcriptomics, binding assays, and overexpression, support the hypothesized function of these candidate genes in the P. trichocarpa response to S. musiva.

AB - Invasive microbes causing diseases such as sudden oak death negatively affect ecosystems and economies around the world. The deployment of resistant genotypes for combating introduced diseases typically relies on breeding programs that can take decades to complete. To demonstrate how this process can be accelerated, we employed a genome-wide association mapping of ca. 1,000 resequenced Populus trichocarpa trees individually challenged with Sphaerulina musiva, an invasive fungal pathogen. Among significant associations, three loci associated with resistancewere identified and predicted to encode one putative membrane-bound L-type receptorlike kinase and two receptor-like proteins. A susceptibility-associated locus was predicted to encode a putative G-type D-mannose-binding receptor-like kinase. Multiple lines of evidence, including allele analysis, transcriptomics, binding assays, and overexpression, support the hypothesized function of these candidate genes in the P. trichocarpa response to S. musiva.

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KW - Disease resistance

KW - Invasive disease

KW - Populus trichocarpa

KW - Septoria canker

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U2 - 10.1073/pnas.1804428115

DO - 10.1073/pnas.1804428115

M3 - Article

C2 - 30337484

AN - SCOPUS:85056133469

SN - 0027-8424

VL - 115

SP - 11573

EP - 11578

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 45

ER -

Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree

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Keywords

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