Zymoseptoria tritici white-collar complex integrates light, temperature and plant cues to initiate dimorphism and pathogenesis

Sreedhar Kilaru; Elena Fantozzi; Stuart Cannon; Martin Schuster; Thomas M. Chaloner; Celia Guiu-Aragones; Sarah J. Gurr; Gero Steinberg

doi:10.1038/s41467-022-33183-2

Zymoseptoria tritici white-collar complex integrates light, temperature and plant cues to initiate dimorphism and pathogenesis

Sreedhar Kilaru, Elena Fantozzi, Stuart Cannon, Martin Schuster, Thomas M. Chaloner, Celia Guiu-Aragones, Sarah J. Gurr, Gero Steinberg

University of Exeter

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

Abstract

Transitioning from spores to hyphae is pivotal to host invasion by the plant pathogenic fungus Zymoseptoria tritici. This dimorphic switch can be initiated by high temperature in vitro (~27 °C); however, such a condition may induce cellular heat stress, questioning its relevance to field infections. Here, we study the regulation of the dimorphic switch by temperature and other factors. Climate data from wheat-growing areas indicate that the pathogen sporadically experiences high temperatures such as 27 °C during summer months. However, using a fluorescent dimorphic switch reporter (FDR1) in four wild-type strains, we show that dimorphic switching already initiates at 15-18 °C, and is enhanced by wheat leaf surface compounds. Transcriptomics reveals 1261 genes that are up- or down-regulated in hyphae of all strains. These pan-strain core dimorphism genes (PCDGs) encode known effectors, dimorphism and transcription factors, and light-responsive proteins (velvet factors, opsins, putative blue light receptors). An FDR1-based genetic screen reveals a crucial role for the white-collar complex (WCC) in dimorphism and virulence, mediated by control of PCDG expression. Thus, WCC integrates light with biotic and abiotic cues to orchestrate Z. tritici infection.

Original language	English
Article number	5625
Number of pages	21
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-33183-2
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
This work was funded by the British Biotechnology and Biological Sciences Research Council, grant BB/P018335/1 awarded to principal investigator G.S. and co-investigator S.J.G. We thank Prof. Bruce McDonald, ETH Zürich, Prof. Gert Kema, Wageningen University and Dr Helen Fones, Exeter University, for their kind provision of wildtype Z. tritici strains 1E4, T5 and MC2306, respectively. The authors are grateful to Andy Early and Connor Simpson for performing plant-infection assays, and Weibin Ma, Lau Siu Hin, Ian Leaves and Rachael Murray for technical support. Prof. Deborah Bell-Pedersen is acknowledged for discussions and the idea to test pathogenicity in asynchronous light conditions. We are most grateful to Prof. Nicholas Smirnoff and Debbie Salmon, both from the Mass Spectrometry Facility, Exeter University, for performing the GC-MS analysis and for their help with interpretation. We would like to thank the Exeter Sequencing Service, for sequencing the genomes of the wildtype strains and the transcriptomes. Finally, we wish to express our gratitude to the anonymous referees; their critical assessments improved this manuscript considerably. S.J.G. is a CIFAR fellow of the research programme The Fungal Kingdom: Threats and Opportunities.

Funding Information:
This work was funded by the British Biotechnology and Biological Sciences Research Council, grant BB/P018335/1 awarded to principal investigator G.S. and co-investigator S.J.G. We thank Prof. Bruce McDonald, ETH Zürich, Prof. Gert Kema, Wageningen University and Dr Helen Fones, Exeter University, for their kind provision of wildtype Z. tritici strains 1E4, T5 and MC2306, respectively. The authors are grateful to Andy Early and Connor Simpson for performing plant-infection assays, and Weibin Ma, Lau Siu Hin, Ian Leaves and Rachael Murray for technical support. Prof. Deborah Bell-Pedersen is acknowledged for discussions and the idea to test pathogenicity in asynchronous light conditions. We are most grateful to Prof. Nicholas Smirnoff and Debbie Salmon, both from the Mass Spectrometry Facility, Exeter University, for performing the GC-MS analysis and for their help with interpretation. We would like to thank the Exeter Sequencing Service, for sequencing the genomes of the wildtype strains and the transcriptomes. Finally, we wish to express our gratitude to the anonymous referees; their critical assessments improved this manuscript considerably. S.J.G. is a CIFAR fellow of the research programme The Fungal Kingdom: Threats and Opportunities.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Fluorescent markers
Fungal
Gene
Growth
Mycosphaerella-graminicola
Neurospora-crassa
Pathogenicity
Protein
Transcription factor
Wheat

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title = "Zymoseptoria tritici white-collar complex integrates light, temperature and plant cues to initiate dimorphism and pathogenesis",

abstract = "Transitioning from spores to hyphae is pivotal to host invasion by the plant pathogenic fungus Zymoseptoria tritici. This dimorphic switch can be initiated by high temperature in vitro (~27 °C); however, such a condition may induce cellular heat stress, questioning its relevance to field infections. Here, we study the regulation of the dimorphic switch by temperature and other factors. Climate data from wheat-growing areas indicate that the pathogen sporadically experiences high temperatures such as 27 °C during summer months. However, using a fluorescent dimorphic switch reporter (FDR1) in four wild-type strains, we show that dimorphic switching already initiates at 15-18 °C, and is enhanced by wheat leaf surface compounds. Transcriptomics reveals 1261 genes that are up- or down-regulated in hyphae of all strains. These pan-strain core dimorphism genes (PCDGs) encode known effectors, dimorphism and transcription factors, and light-responsive proteins (velvet factors, opsins, putative blue light receptors). An FDR1-based genetic screen reveals a crucial role for the white-collar complex (WCC) in dimorphism and virulence, mediated by control of PCDG expression. Thus, WCC integrates light with biotic and abiotic cues to orchestrate Z. tritici infection.",

keywords = "Fluorescent markers, Fungal, Gene, Growth, Mycosphaerella-graminicola, Neurospora-crassa, Pathogenicity, Protein, Transcription factor, Wheat",

author = "Sreedhar Kilaru and Elena Fantozzi and Stuart Cannon and Martin Schuster and Chaloner, {Thomas M.} and Celia Guiu-Aragones and Gurr, {Sarah J.} and Gero Steinberg",

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AU - Cannon, Stuart

AU - Schuster, Martin

AU - Chaloner, Thomas M.

AU - Guiu-Aragones, Celia

AU - Gurr, Sarah J.

AU - Steinberg, Gero

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N2 - Transitioning from spores to hyphae is pivotal to host invasion by the plant pathogenic fungus Zymoseptoria tritici. This dimorphic switch can be initiated by high temperature in vitro (~27 °C); however, such a condition may induce cellular heat stress, questioning its relevance to field infections. Here, we study the regulation of the dimorphic switch by temperature and other factors. Climate data from wheat-growing areas indicate that the pathogen sporadically experiences high temperatures such as 27 °C during summer months. However, using a fluorescent dimorphic switch reporter (FDR1) in four wild-type strains, we show that dimorphic switching already initiates at 15-18 °C, and is enhanced by wheat leaf surface compounds. Transcriptomics reveals 1261 genes that are up- or down-regulated in hyphae of all strains. These pan-strain core dimorphism genes (PCDGs) encode known effectors, dimorphism and transcription factors, and light-responsive proteins (velvet factors, opsins, putative blue light receptors). An FDR1-based genetic screen reveals a crucial role for the white-collar complex (WCC) in dimorphism and virulence, mediated by control of PCDG expression. Thus, WCC integrates light with biotic and abiotic cues to orchestrate Z. tritici infection.

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Zymoseptoria tritici white-collar complex integrates light, temperature and plant cues to initiate dimorphism and pathogenesis

Abstract

Bibliographical note

Keywords

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