Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses

Elisabet Sjokvist; Rene Lemcke; Manoj Kamble; Frances Turner; Mark Blaxter; Neil H.D. Havis; Michael F. Lyngkjær; Simona Radutoiu

doi:10.1094/mpmi-05-18-0113-r

Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses

Elisabet Sjokvist, Rene Lemcke, Manoj Kamble, Frances Turner, Mark Blaxter, Neil H.D. Havis, Michael F. Lyngkjær, Simona Radutoiu^*

^*Corresponding author for this work

Section for Plant Biochemistry

4 Citations (Scopus)

Abstract

Ramularia leaf spot disease (RLS), caused by the ascomycete fungus Ramularia collo-cygni, has emerged as a major economic disease of barley. No substantial resistance has been identified, so far, among barley genotypes and, based on the epidemiology of the disease, a quantitative genetic determinacy of RLS has been suggested. The relative contributions of barley and R. collo-cygni genetics to disease infection and epidemiology are practically unknown. Here, we present an integrated genome-wide analysis of host and pathogen transcriptome landscapes identified in a sensitive barley cultivar following infection by an aggressive R. collo-cygni isolate. We compared transcriptional responses in the infected and noninfected leaf samples in order to identify which molecular events are associated with RLS symptom development. We found a large proportion of R. collo-cygni genes to be expressed in planta and that many were also closely associated with the infection stage. The transition from surface to apoplastic colonization was associated with downregulation of cell wall–degrading genes and upregulation of nutrient uptake and resistance to oxidative stresses. Interestingly, the production of secondary metabolites was dynamically regulated within the fungus, indicating that R. collo-cygni produces a diverse panel of toxic compounds according to the infection stage. A defense response against R. collo-cygni was identified in barley at the early, asymptomatic infection and colonization stages. We found activation of ethylene signaling, jasmonic acid signaling, and phenylpropanoid and flavonoid pathways to be highly induced, indicative of a classical response to necrotrophic pathogens. Disease development was found to be associated with geneexpression patterns similar to those found at the onset of leaf senescence, when nutrients, possibly, are used by the infecting fungus. These analyses, combining both barley and R. collocygni transcript profiles, demonstrate the activation of complex transcriptional programs in both organisms.

Original language	English
Journal	Molecular Plant-Microbe Interactions
Volume	32
Issue number	2
Pages (from-to)	176-193
Number of pages	18
ISSN	0894-0282
DOIs	https://doi.org/10.1094/mpmi-05-18-0113-r
Publication status	Published - 1 Feb 2019

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title = "Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses",

abstract = "Ramularia leaf spot disease (RLS), caused by the ascomycete fungus Ramularia collo-cygni, has emerged as a major economic disease of barley. No substantial resistance has been identified, so far, among barley genotypes and, based on the epidemiology of the disease, a quantitative genetic determinacy of RLS has been suggested. The relative contributions of barley and R. collo-cygni genetics to disease infection and epidemiology are practically unknown. Here, we present an integrated genome-wide analysis of host and pathogen transcriptome landscapes identified in a sensitive barley cultivar following infection by an aggressive R. collo-cygni isolate. We compared transcriptional responses in the infected and noninfected leaf samples in order to identify which molecular events are associated with RLS symptom development. We found a large proportion of R. collo-cygni genes to be expressed in planta and that many were also closely associated with the infection stage. The transition from surface to apoplastic colonization was associated with downregulation of cell wall–degrading genes and upregulation of nutrient uptake and resistance to oxidative stresses. Interestingly, the production of secondary metabolites was dynamically regulated within the fungus, indicating that R. collo-cygni produces a diverse panel of toxic compounds according to the infection stage. A defense response against R. collo-cygni was identified in barley at the early, asymptomatic infection and colonization stages. We found activation of ethylene signaling, jasmonic acid signaling, and phenylpropanoid and flavonoid pathways to be highly induced, indicative of a classical response to necrotrophic pathogens. Disease development was found to be associated with geneexpression patterns similar to those found at the onset of leaf senescence, when nutrients, possibly, are used by the infecting fungus. These analyses, combining both barley and R. collocygni transcript profiles, demonstrate the activation of complex transcriptional programs in both organisms.",

author = "Elisabet Sjokvist and Rene Lemcke and Manoj Kamble and Frances Turner and Mark Blaxter and Havis, {Neil H.D.} and Lyngkj{\ae}r, {Michael F.} and Simona Radutoiu",

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T1 - Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses

AU - Sjokvist, Elisabet

AU - Lemcke, Rene

AU - Kamble, Manoj

AU - Turner, Frances

AU - Blaxter, Mark

AU - Havis, Neil H.D.

AU - Lyngkjær, Michael F.

AU - Radutoiu, Simona

PY - 2019/2/1

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N2 - Ramularia leaf spot disease (RLS), caused by the ascomycete fungus Ramularia collo-cygni, has emerged as a major economic disease of barley. No substantial resistance has been identified, so far, among barley genotypes and, based on the epidemiology of the disease, a quantitative genetic determinacy of RLS has been suggested. The relative contributions of barley and R. collo-cygni genetics to disease infection and epidemiology are practically unknown. Here, we present an integrated genome-wide analysis of host and pathogen transcriptome landscapes identified in a sensitive barley cultivar following infection by an aggressive R. collo-cygni isolate. We compared transcriptional responses in the infected and noninfected leaf samples in order to identify which molecular events are associated with RLS symptom development. We found a large proportion of R. collo-cygni genes to be expressed in planta and that many were also closely associated with the infection stage. The transition from surface to apoplastic colonization was associated with downregulation of cell wall–degrading genes and upregulation of nutrient uptake and resistance to oxidative stresses. Interestingly, the production of secondary metabolites was dynamically regulated within the fungus, indicating that R. collo-cygni produces a diverse panel of toxic compounds according to the infection stage. A defense response against R. collo-cygni was identified in barley at the early, asymptomatic infection and colonization stages. We found activation of ethylene signaling, jasmonic acid signaling, and phenylpropanoid and flavonoid pathways to be highly induced, indicative of a classical response to necrotrophic pathogens. Disease development was found to be associated with geneexpression patterns similar to those found at the onset of leaf senescence, when nutrients, possibly, are used by the infecting fungus. These analyses, combining both barley and R. collocygni transcript profiles, demonstrate the activation of complex transcriptional programs in both organisms.

AB - Ramularia leaf spot disease (RLS), caused by the ascomycete fungus Ramularia collo-cygni, has emerged as a major economic disease of barley. No substantial resistance has been identified, so far, among barley genotypes and, based on the epidemiology of the disease, a quantitative genetic determinacy of RLS has been suggested. The relative contributions of barley and R. collo-cygni genetics to disease infection and epidemiology are practically unknown. Here, we present an integrated genome-wide analysis of host and pathogen transcriptome landscapes identified in a sensitive barley cultivar following infection by an aggressive R. collo-cygni isolate. We compared transcriptional responses in the infected and noninfected leaf samples in order to identify which molecular events are associated with RLS symptom development. We found a large proportion of R. collo-cygni genes to be expressed in planta and that many were also closely associated with the infection stage. The transition from surface to apoplastic colonization was associated with downregulation of cell wall–degrading genes and upregulation of nutrient uptake and resistance to oxidative stresses. Interestingly, the production of secondary metabolites was dynamically regulated within the fungus, indicating that R. collo-cygni produces a diverse panel of toxic compounds according to the infection stage. A defense response against R. collo-cygni was identified in barley at the early, asymptomatic infection and colonization stages. We found activation of ethylene signaling, jasmonic acid signaling, and phenylpropanoid and flavonoid pathways to be highly induced, indicative of a classical response to necrotrophic pathogens. Disease development was found to be associated with geneexpression patterns similar to those found at the onset of leaf senescence, when nutrients, possibly, are used by the infecting fungus. These analyses, combining both barley and R. collocygni transcript profiles, demonstrate the activation of complex transcriptional programs in both organisms.

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U2 - 10.1094/mpmi-05-18-0113-r

DO - 10.1094/mpmi-05-18-0113-r

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AN - SCOPUS:85060517336

SN - 0894-0282

VL - 32

SP - 176

EP - 193

JO - Molecular Plant-Microbe Interactions

JF - Molecular Plant-Microbe Interactions

IS - 2

ER -

Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses

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