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

• Published in: Nature communications 2022-09, Vol.13 (1), p.5625-21, Article 5625
• Main Authors: Kilaru, Sreedhar, Fantozzi, Elena, Cannon, Stuart, Schuster, Martin, Chaloner, Thomas M., Guiu-Aragones, Celia, Gurr, Sarah J., Steinberg, Gero
• Format: Article
• Language: English
• Subjects: 14; 14/19; 14/35; 38; 38/23; 38/39; 38/90; 38/91; 45/70; 45/77; 631/326/193/2542; 631/326/421; 631/326/88; 631/449; Ascomycota; Climatic data; Cues; Dimorphism; Fluorescence; Fungi; Gene expression; Genes; Genetic screening; Heat; Heat stress; Heat tolerance; High temperature; Host plants; Humanities and Social Sciences; Hyphae; Infections; Leaves; Light; multidisciplinary; Opsins; Pathogenesis; Pathogens; Plant Diseases - microbiology; Proteins; Science; Science (multidisciplinary); Sex Characteristics; Spores; Stomata; Temperature; Transcription Factors; Transcriptomics; Triticum - genetics; Triticum - microbiology; Virulence; Wheat; Zymoseptoria tritici
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-022-33183-2

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. Transitioning from spores to hyphae is crucial for host invasion by the plant pathogenic fungus Zymoseptoria tritici . Here, the authors show that the spore-to-hypha transition is enhanced by wheat leaf surface compounds and is regulated by the white-collar complex, which integrates light with biotic and abiotic cues to allow host invasion through open stomata.