Regulation of Stomatal Tropism and Infection by Light in Cercospora zeae-maydis: Evidence for Coordinated Host/Pathogen Responses to Photoperiod?

Abstract

Cercospora zeae-maydis causes gray leaf spot of maize, which has become one of the most widespread and destructive diseases of maize in the world. C. zeae-maydis infects leaves through stomata, which is predicated on the ability of the pathogen to perceive stomata and reorient growth accordingly. In this study, the discovery that light was required for C. zeae-maydis to perceive stomata and infect leaves led to the identification of CRP1, a gene encoding a putative blue-light photoreceptor homologous to White Collar-1 (WC-1) of Neurospora crassa. Disrupting CRP1 via homologous recombination revealed roles in multiple aspects of pathogenesis, including tropism of hyphae to stomata, the formation of appressoria, conidiation, and the biosynthesis of cercosporin. CRP1 was also required for photoreactivation after lethal doses of UV exposure. Intriguingly, putative orthologs of CRP1 are central regulators of circadian clocks in other filamentous fungi, raising the possibility that C. zeae-maydis uses light as a key environmental input to coordinate pathogenesis with maize photoperiodic responses. This study identified a novel molecular mechanism underlying stomatal tropism in a foliar fungal pathogen, provides specific insight into how light regulates pathogenesis in C. zeae-maydis, and establishes a genetic framework for the molecular dissection of infection via stomata and the integration of host and pathogen responses to photoperiod.

Fungal photobiology: visible light as a signal for stress, space and time

“…loss of light-induced gene expression upon deletion of the wc-1 and wc-2 orthologs. However, in contrast to Neurospora in which the WCC is thought to serve almost exclusively as a transcriptional activator, it is thought to have repressive roles in other species including A. nidulans (Bayram et al 2010), Alternaria alternata (Pruβ et al 2014), Trichoderma reesei (Tisch and Schmoll 2013), Trichoderma atroviride (Sanchez-Arreguin et al 2012), Fusarium graminearum (Kim et al 2014a) and Cercospora zae-maydis (Kim et al 2011a). Interestingly, deletion of the wc-1 ortholog in Trichoderma atroviride leads to a broad down-regulation of proteins in the dark whereas deletion of wc -2 leads predominantly to protein up-regulation, indicating independent functions for the two proteins (Sanchez-Arreguin et al 2012).…”

“…Conversely, blue and/or red light represses asexual development in Aspergillus oryzae (blue and red)(Hatakeyama et al 2007), Alternaria alternata (blue, and to a lesser extent, red) (Pruβ et al 2014, Lukens 1965), Magnaporthe oryzae (blue) (Lee et al 2006) and Cercospera zeae-maydis (blue)(Kim et al 2011a). In the case of M. oryzae , A. alternata and C. zeae-maydis , loss of the wc-1 ortholog leads to a de-repression of conidiation in light.…”

“…Conversely, light represses infectivity in the rice blast pathogen Magnaporthe oryzae and this repression is dependent upon the wc-1 ortholog (Kim et al 2011b). Moreover, the deletion of the wc-1 ortholog leads to attenuated virulence in the gray mold pathogen Botrytis cinerea (Canessa et al 2013) and the maize leaf pathogen Cercospora zae-maydis (Kim et al 2011a). Similarly, and perhaps more surprisingly, deletion of the wc-1 ortholog also attenuates virulence in two human fungal pathogens, the basidiomycete yeast Cryptococcus neoformans (Idnurm and Heitman 2005a) and the ascomycete mold Fusarium oxysporum (Ruiz-Roldan et al 2008).…”

Seeing the world differently: variability in the photosensory mechanisms of two model fungi

“…However, understanding photobiology may have merit in its own right, as the importance of light on agriculturally, industrially and even medically important fungi becomes appreciated. For example, light enhances plant lesion size during infection with Colletotrichum acutatum and Cercospora zeae-maydis , but represses infection with Magnaporthe oryzae (Kim et al , 2011a; Kim et al , 2011b; Yu et al , 2013). It is difficult to dissect the influence of light on the pathogen versus the host in these experiments, but at least in the case of M. oryzae , the light effect is lost upon deletion of wc-1 .…”

“…It is difficult to dissect the influence of light on the pathogen versus the host in these experiments, but at least in the case of M. oryzae , the light effect is lost upon deletion of wc-1 . Moreover, wc-1 deletion attenuates virulence in both Botrytis cinerea (Canessa et al , 2013) and C. zeae-maydis (Kim et al , 2011a) and, incredibly, in two distantly related human pathogens, Cryptococcus neoformans (Idnurm and Heitman, 2005) and Fusarium oxysporum (Ruiz-Roldan et al , 2008). …”