Zymoseptoria tritici white-collar complex integrates light, temperature and plant cues to initiate dimorphism and pathogenesis
Kilaru, Sreedhar; Fantozzi, Elena; Cannon, Stuart; Schuster, Martin; Chaloner, Thomas M.; Guiu-Aragones, Celia; Gurr, Sarah J.; Steinberg, Gero
(2022) Nature Communications, volume 13, issue 1
(Article)
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
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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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Keywords: Fluorescent markers, Fungal, Gene, Growth, Mycosphaerella-graminicola, Neurospora-crassa, Pathogenicity, Protein, Transcription factor, Wheat, General, General Physics and Astronomy, General Chemistry, General Biochemistry,Genetics and Molecular Biology
ISSN: 2041-1723
Publisher: Nature Publishing Group
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).
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