Differential Regulation of Maize and Sorghum Orthologs in Response to the Fungal Pathogen Exserohilum turcicum
Abstract
Pathogens that infect more than one host offer an opportunity to study how resistance mechanisms have evolved across different species.Exserohilum turcicuminfects both maize and sorghum and the isolates are host-specific, offering a unique system to examine both compatible and incompatible interactions. We conducted transcriptional analysis of maize and sorghum in response to maize-specific and sorghum-specificE. turcicumisolates and identified functionally related co-expressed modules. Maize had a more robust transcriptional response than sorghum.E. turcicumresponsive genes were enriched in core orthologs in both crops, but only up to 16% of core orthologs showed conserved expression patterns. Most changes in gene expression for the core orthologs, including hub genes, were lineage specific, suggesting a role for regulatory divergent evolution. We identified several defense-related shared differentially expressed (DE) orthologs with conserved expression patterns between the two crops, suggesting a role for parallel evolution of those genes in both crops. Many of the differentially expressed genes (DEGs) during the incompatible interaction were related to quantitative disease resistance (QDR). This work offers insights into how different hosts with relatively recent divergence interact with a common pathogen. Our results are important for developing resistance to this critical pathogen and understanding the evolution of host-pathogen interactions.
- Authors:
-
- Univ. of Illinois at Urbana-Champaign, IL (United States). Dept. of Crop Sciences
- Publication Date:
- Research Org.:
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1852922
- Grant/Contract Number:
- SC0019189
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 12; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Plant Sciences; quantitative disease resistance; transcriptome; host resistance; maize (Zea mays L.); sorghum; Exserohilum turcicum
Citation Formats
Adhikari, Pragya, Mideros, Santiago X., and Jamann, Tiffany M. Differential Regulation of Maize and Sorghum Orthologs in Response to the Fungal Pathogen Exserohilum turcicum. United States: N. p., 2021.
Web. doi:10.3389/fpls.2021.675208.
Adhikari, Pragya, Mideros, Santiago X., & Jamann, Tiffany M. Differential Regulation of Maize and Sorghum Orthologs in Response to the Fungal Pathogen Exserohilum turcicum. United States. https://doi.org/10.3389/fpls.2021.675208
Adhikari, Pragya, Mideros, Santiago X., and Jamann, Tiffany M. Tue .
"Differential Regulation of Maize and Sorghum Orthologs in Response to the Fungal Pathogen Exserohilum turcicum". United States. https://doi.org/10.3389/fpls.2021.675208. https://www.osti.gov/servlets/purl/1852922.
@article{osti_1852922,
title = {Differential Regulation of Maize and Sorghum Orthologs in Response to the Fungal Pathogen Exserohilum turcicum},
author = {Adhikari, Pragya and Mideros, Santiago X. and Jamann, Tiffany M.},
abstractNote = {Pathogens that infect more than one host offer an opportunity to study how resistance mechanisms have evolved across different species.Exserohilum turcicuminfects both maize and sorghum and the isolates are host-specific, offering a unique system to examine both compatible and incompatible interactions. We conducted transcriptional analysis of maize and sorghum in response to maize-specific and sorghum-specificE. turcicumisolates and identified functionally related co-expressed modules. Maize had a more robust transcriptional response than sorghum.E. turcicumresponsive genes were enriched in core orthologs in both crops, but only up to 16% of core orthologs showed conserved expression patterns. Most changes in gene expression for the core orthologs, including hub genes, were lineage specific, suggesting a role for regulatory divergent evolution. We identified several defense-related shared differentially expressed (DE) orthologs with conserved expression patterns between the two crops, suggesting a role for parallel evolution of those genes in both crops. Many of the differentially expressed genes (DEGs) during the incompatible interaction were related to quantitative disease resistance (QDR). This work offers insights into how different hosts with relatively recent divergence interact with a common pathogen. Our results are important for developing resistance to this critical pathogen and understanding the evolution of host-pathogen interactions.},
doi = {10.3389/fpls.2021.675208},
journal = {Frontiers in Plant Science},
number = ,
volume = 12,
place = {United States},
year = {Tue May 25 00:00:00 EDT 2021},
month = {Tue May 25 00:00:00 EDT 2021}
}
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Works referenced in this record:
Over-expression of an S-domain receptor-like kinase extracellular domain improves panicle architecture and grain yield in rice
journal, October 2015
- Zou, Xiaohua; Qin, Zhengrui; Zhang, Chunyu
- Journal of Experimental Botany, Vol. 66, Issue 22
Plant pathogens and integrated defence responses to infection
journal, June 2001
- Dangl, Jeffery L.; Jones, Jonathan D. G.
- Nature, Vol. 411, Issue 6839
Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana
journal, July 2009
- Zou, Cheng; Lehti-Shiu, Melissa D.; Thomashow, Michael
- PLoS Genetics, Vol. 5, Issue 7
The Sorghum bicolor genome and the diversification of grasses
journal, January 2009
- Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
- Nature, Vol. 457, Issue 7229
RNA sequencing-based transcriptome analysis of mature strawberry fruit infected by necrotrophic fungal pathogen Botrytis cinerea
journal, December 2018
- Xiong, Jin-Song; Zhu, Hong-Yu; Bai, Yi-Bo
- Physiological and Molecular Plant Pathology, Vol. 104
Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population
journal, January 2011
- Kump, Kristen L.; Bradbury, Peter J.; Wisser, Randall J.
- Nature Genetics, Vol. 43, Issue 2
STAR: ultrafast universal RNA-seq aligner
journal, October 2012
- Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
- Bioinformatics, Vol. 29, Issue 1
Evaluation of Sorghum [Sorghum bicolor (L.)] Reference Genes in Various Tissues and under Abiotic Stress Conditions for Quantitative Real-Time PCR Data Normalization
journal, April 2016
- Sudhakar Reddy, Palakolanu; Srinivas Reddy, Dumbala; Sivasakthi, Kaliamoorthy
- Frontiers in Plant Science, Vol. 7
Analyzing real-time PCR data by the comparative CT method
journal, June 2008
- Schmittgen, Thomas D.; Livak, Kenneth J.
- Nature Protocols, Vol. 3, Issue 6
Weighted gene co-expression network analysis unveils gene networks associated with the Fusarium head blight resistance in tetraploid wheat
journal, December 2019
- Sari, Ehsan; Cabral, Adrian L.; Polley, Brittany
- BMC Genomics, Vol. 20, Issue 1
XV.—The Correlation between Relatives on the Supposition of Mendelian Inheritance.
journal, January 1919
- Fisher, R. A.
- Transactions of the Royal Society of Edinburgh, Vol. 52, Issue 2
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
The Evolution of Gene Expression in cis and trans
journal, July 2018
- Signor, Sarah A.; Nuzhdin, Sergey V.
- Trends in Genetics, Vol. 34, Issue 7
Quantitative Resistance: More Than Just Perception of a Pathogen
journal, March 2017
- Corwin, Jason A.; Kliebenstein, Daniel J.
- The Plant Cell, Vol. 29, Issue 4
The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase
journal, June 2015
- Hurni, Severine; Scheuermann, Daniela; Krattinger, Simon G.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 28
Corn Yield Loss Estimates Due to Diseases in the United States and Ontario, Canada from 2012 to 2015
journal, January 2016
- Mueller, Daren S.; Wise, Kiersten A.; Sisson, Adam J.
- Plant Health Progress, Vol. 17, Issue 3
Overlapping Yet Response-Specific Transcriptome Alterations Characterize the Nature of Tobacco–Pseudomonas syringae Interactions
journal, March 2016
- Bozsó, Zoltán; Ott, Péter G.; Kámán-Tóth, Evelin
- Frontiers in Plant Science, Vol. 7
Resistance to phytopathogens e tutti quanti : placing plant quantitative disease resistance on the map: Quantitative disease resistance in plants
journal, May 2014
- Roux, Fabrice; Voisin, Derry; Badet, Thomas
- Molecular Plant Pathology, Vol. 15, Issue 5
Genetic Structure of Setosphaeria turcica Populations in Tropical and Temperate Climates
journal, April 1998
- Borchardt, Dorothea S.; Welz, H. Günter; Geiger, Hartwig H.
- Phytopathology, Vol. 88, Issue 4
Inheritance of Pathogenicity in Setosphaeria turcica
journal, January 1975
- Hamid, Ali H.
- Phytopathology, Vol. 65, Issue 3
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21
journal, December 1995
- Song, W. -Y.; Wang, G. -L.; Chen, L. -L.
- Science, Vol. 270, Issue 5243
Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea.
journal, January 1997
- Pastuglia, M.; Roby, D.; Dumas, C.
- The Plant Cell, Vol. 9, Issue 1
The Quantitative Basis of the Arabidopsis Innate Immune System to Endemic Pathogens Depends on Pathogen Genetics
journal, February 2016
- Corwin, Jason A.; Copeland, Daniel; Feusier, Julie
- PLOS Genetics, Vol. 12, Issue 2
DNA sequence evidence for the segmental allotetraploid origin of maize
journal, June 1997
- Gaut, B. S.; Doebley, J. F.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 13
A highly conserved NB-LRR encoding gene cluster effective against Setosphaeria turcica in sorghum
journal, January 2011
- Martin, Tom; Biruma, Moses; Fridborg, Ingela
- BMC Plant Biology, Vol. 11, Issue 1
Comparative Transcriptome Analysis Reveals Key Pathways and Hub Genes in Rapeseed During the Early Stage of Plasmodiophora brassicae Infection
journal, January 2020
- Li, Lixia; Long, Ying; Li, Hao
- Frontiers in Genetics, Vol. 10
Pivoting the Plant Immune System from Dissection to Deployment
journal, August 2013
- Dangl, J. L.; Horvath, D. M.; Staskawicz, B. J.
- Science, Vol. 341, Issue 6147
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
Resistance to Foliar Diseases in a Mini-Core Collection of Sorghum Germplasm
journal, November 2012
- Sharma, Rajan; Upadhyaya, H. D.; Manjunatha, S. V.
- Plant Disease, Vol. 96, Issue 11
Genetic differentiation in populations of Exserohilum turcicum from maize and sorghum in South Africa
journal, May 2018
- Nieuwoudt, A.; Human, M. P.; Craven, M.
- Plant Pathology, Vol. 67, Issue 7
Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq
journal, January 2013
- Zhu, Qian-Hao; Stephen, Stuart; Kazan, Kemal
- Gene, Vol. 512, Issue 2
An Expanded View of Complex Traits: From Polygenic to Omnigenic
journal, June 2017
- Boyle, Evan A.; Li, Yang I.; Pritchard, Jonathan K.
- Cell, Vol. 169, Issue 7
A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat
journal, November 2015
- Moore, John W.; Herrera-Foessel, Sybil; Lan, Caixia
- Nature Genetics, Vol. 47, Issue 12
Andropogoneae Evolution and Generic Limits in Sorghum (Poaceae) Using ndhF Sequences
journal, April 1999
- Spangler, Russ; Zaitchik, Ben; Russo, Elizabeth
- Systematic Botany, Vol. 24, Issue 2
Regulation of sugar transporter activity for antibacterial defense in Arabidopsis
journal, November 2016
- Yamada, Kohji; Saijo, Yusuke; Nakagami, Hirofumi
- Science, Vol. 354, Issue 6318
Directional Selection from Host Plants Is a Major Force Driving Host Specificity in Magnaporthe Species
journal, May 2016
- Zhong, Zhenhui; Norvienyeku, Justice; Chen, Meilian
- Scientific Reports, Vol. 6, Issue 1
Grass Syntenic Gene List sorghum v3 maize v3/4 with teff and oropetium v2
dataset, January 2019
- Schnable, James
- figshare
Resistance to anthracnose and turcicum leaf blight in sorghum under dual infection
journal, April 2016
- Beshir, Mayada M.; Okori, Patrick; Ahmed, Nafisa E.
- Plant Breeding, Vol. 135, Issue 3
A century after Fisher: time for a new paradigm in quantitative genetics
journal, December 2013
- Nelson, Ronald M.; Pettersson, Mats E.; Carlborg, Örjan
- Trends in Genetics, Vol. 29, Issue 12
A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010
- Robinson, Mark D.; Oshlack, Alicia
- Genome Biology, Vol. 11, Issue 3, Article No. R25
Conserved defense responses between maize and sorghum to Exserohilum turcicum
journal, February 2020
- Zhang, Xiaoyue; Fernandes, Samuel B.; Kaiser, Christopher
- BMC Plant Biology, Vol. 20, Issue 1
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
Maize Homologs of HCT, a Key Enzyme in Lignin Biosynthesis, Bind the NLR Rp1 Proteins to Modulate the Defense Response
journal, September 2015
- Wang, Guan-Feng; He, Yijian; Strauch, Renee
- Plant Physiology
Shades of gray: the world of quantitative disease resistance
journal, January 2009
- Poland, Jesse A.; Balint-Kurti, Peter J.; Wisser, Randall J.
- Trends in Plant Science, Vol. 14, Issue 1
Pattern Triggered Immunity (PTI) in Tobacco: Isolation of Activated Genes Suggests Role of the Phenylpropanoid Pathway in Inhibition of Bacterial Pathogens
journal, August 2014
- Szatmári, Ágnes; Zvara, Ágnes; Móricz, Ágnes M.
- PLoS ONE, Vol. 9, Issue 8
Transgenic Tomato Plants Overexpressing Tyramine N -Hydroxycinnamoyltransferase Exhibit Elevated Hydroxycinnamic Acid Amide Levels and Enhanced Resistance to Pseudomonas syringae
journal, October 2014
- Campos, Laura; Lisón, Purificación; López-Gresa, María Pilar
- Molecular Plant-Microbe Interactions®, Vol. 27, Issue 10
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update
journal, May 2017
- Tian, Tian; Liu, Yue; Yan, Hengyu
- Nucleic Acids Research, Vol. 45, Issue W1
Transcriptional Profiling of Rice Early Response to Magnaporthe oryzae Identified OsWRKYs as Important Regulators in Rice Blast Resistance
journal, March 2013
- Wei, Tong; Ou, Bin; Li, Jinbin
- PLoS ONE, Vol. 8, Issue 3
Genetics of Resistance and Pathogenicity in the Maize/Setosphaeria turcica Pathosystem and Implications for Breeding
journal, August 2017
- Galiano-Carneiro, Ana L.; Miedaner, Thomas
- Frontiers in Plant Science, Vol. 8
The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel
journal, January 2018
- Shi, Xuetao; Long, Yu; He, Feng
- PLOS Pathogens, Vol. 14, Issue 1
Differentially Regulated Orthologs in Sorghum and the Subgenomes of Maize
journal, July 2017
- Zhang, Yang; Ngu, Daniel W.; Carvalho, Daniel
- The Plant Cell, Vol. 29, Issue 8
Regulatory changes underlying expression differences within and between Drosophila species
journal, February 2008
- Wittkopp, Patricia J.; Haerum, Belinda K.; Clark, Andrew G.
- Nature Genetics, Vol. 40, Issue 3
Arabidopsis non-host resistance to powdery mildews
journal, August 2008
- Lipka, Ulrike; Fuchs, Rene; Lipka, Volker
- Current Opinion in Plant Biology, Vol. 11, Issue 4
Herbaspirillum rubrisubalbicans as a phytopathogenic model to study the immune system of Sorghum bicolor
journal, November 2019
- Tuleski, Thalita Regina; Kimball, Jennifer; Amaral, Fernanda Plucani do
- Molecular Plant-Microbe Interactions
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009
- Robinson, M. D.; McCarthy, D. J.; Smyth, G. K.
- Bioinformatics, Vol. 26, Issue 1
limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015
- Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
- Nucleic Acids Research, Vol. 43, Issue 7
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
journal, January 2004
- Smyth, Gordon K.
- Statistical Applications in Genetics and Molecular Biology, Vol. 3, Issue 1
Transcriptome analysis of the compatible interaction of tomato with Verticillium dahliae using RNA-sequencing
journal, June 2015
- Tan, Guangxuan; Liu, Kun; Kang, Jingmin
- Frontiers in Plant Science, Vol. 6
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Map-based cloning of a protein kinase gene conferring disease resistance in tomato
journal, November 1993
- Martin, G.; Brommonschenkel, S.; Chunwongse, J.
- Science, Vol. 262, Issue 5138
Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss
journal, February 2011
- Schnable, J. C.; Springer, N. M.; Freeling, M.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 10
One subgenome to rule them all: underlying mechanisms of subgenome dominance
journal, April 2020
- Alger, Elizabeth I.; Edger, Patrick P.
- Current Opinion in Plant Biology, Vol. 54
A remorin gene is implicated in quantitative disease resistance in maize
journal, February 2016
- Jamann, Tiffany M.; Luo, Xingyu; Morales, Laura
- Theoretical and Applied Genetics, Vol. 129, Issue 3
A maize wall-associated kinase confers quantitative resistance to head smut
journal, December 2014
- Zuo, Weiliang; Chao, Qing; Zhang, Nan
- Nature Genetics, Vol. 47, Issue 2
Differential response of tomato genotypes to Xanthomonas-specific pathogen-associated molecular patterns and correlation with bacterial spot (Xanthomonas perforans) resistance
journal, August 2016
- Bhattarai, Krishna; Louws, Frank J.; Williamson, John D.
- Horticulture Research, Vol. 3, Issue 1
Field pathogenomics of Fusarium head blight reveals pathogen transcriptome differences due to host resistance
journal, May 2019
- Fall, Leigh Ann; Salazar, Melissa M.; Drnevich, Jenny
- Mycologia, Vol. 111, Issue 4
Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi
journal, December 2012
- Ohm, Robin A.; Feau, Nicolas; Henrissat, Bernard
- PLoS Pathogens, Vol. 8, Issue 12
Expecting the unexpected: factors influencing the emergence of fungal and oomycete plant pathogens
journal, July 2019
- Corredor‐Moreno, Pilar; Saunders, Diane G. O.
- New Phytologist, Vol. 225, Issue 1
High-efficiency TALEN-based gene editing produces disease-resistant rice
journal, May 2012
- Li, Ting; Liu, Bo; Spalding, Martin H.
- Nature Biotechnology, Vol. 30, Issue 5
Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize - Setosphaeria turcica pathosystem
journal, January 2010
- Chung, Chia-Lin; Longfellow, Joy M.; Walsh, Ellie K.
- BMC Plant Biology, Vol. 10, Issue 1
Detecting novel loci underlying rice blast resistance by integrating a genome-wide association study and RNA sequencing
journal, May 2019
- Lu, Qing; Wang, Caihong; Niu, Xiaojun
- Molecular Breeding, Vol. 39, Issue 6
Phylotranscriptomics of the Pentapetalae Reveals Frequent Regulatory Variation in Plant Local Responses to the Fungal Pathogen Sclerotinia sclerotiorum
journal, April 2020
- Sucher, Justine; Mbengue, Malick; Dresen, Axel
- The Plant Cell, Vol. 32, Issue 6
Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli
journal, June 2013
- Cole, Stephanie J.; Diener, Andrew C.
- New Phytologist, Vol. 200, Issue 1
Close Split of Sorghum and Maize Genome Progenitors
journal, September 2004
- Swigonova, Z.
- Genome Research, Vol. 14, Issue 10a
The B73 Maize Genome: Complexity, Diversity, and Dynamics
journal, November 2009
- Schnable, P. S.; Ware, D.; Fulton, R. S.
- Science, Vol. 326, Issue 5956, p. 1112-1115
Gene co-expression network for Xanthomonas-challenged cassava reveals key regulatory elements of immunity processes
journal, December 2018
- Gómez-Cano, Fabio; Soto, Johana; Restrepo, Silvia
- European Journal of Plant Pathology, Vol. 153, Issue 4
Quantitative Nature of Arabidopsis Responses during Compatible and Incompatible Interactions with the Bacterial Pathogen Pseudomonas syringae
journal, January 2003
- Tao, Yi; Xie, Zhiyi; Chen, Wenqiong
- The Plant Cell, Vol. 15, Issue 2
Parallel vs. Convergent Evolution in Domestication and Diversification of Crops in the Americas
journal, May 2018
- Pickersgill, Barbara
- Frontiers in Ecology and Evolution, Vol. 6
Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat
journal, January 1997
- Feuillet, Catherine; Schachermayr, Gabriele; Keller, Beat
- The Plant Journal, Vol. 11, Issue 1
Robust hyperparameter estimation protects against hypervariable genes and improves power to detect differential expression
journal, June 2016
- Phipson, Belinda; Lee, Stanley; Majewski, Ian J.
- The Annals of Applied Statistics, Vol. 10, Issue 2
p Athogen p Opulation g Enetics , e Volutionary p Otential, and d Urable r Esistance
journal, September 2002
- McDonald, Bruce A.; Linde, Celeste
- Annual Review of Phytopathology, Vol. 40, Issue 1
On the Trail of a Cereal Killer: Exploring the Biology of Magnaporthe grisea
journal, October 2003
- Talbot, Nicholas J.
- Annual Review of Microbiology, Vol. 57, Issue 1
The Genetic Architecture of Disease Resistance in Maize: A Synthesis of Published Studies
journal, February 2006
- Wisser, Randall J.; Balint-Kurti, Peter J.; Nelson, Rebecca J.
- Phytopathology, Vol. 96, Issue 2
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- Zhang, Wenyu; Wang, Zicheng; Dan, Zhencuo
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