Why do some fungi want to be sterile? The role of dysfunctional Pro1 in the rice blast fungus

Abstract

Although sexual reproduction is widespread in eukaryotes, some fungal species can only reproduce asexually. Therefore, loss of sexual reproduction may confer survival advantages under certain conditions in certain species. In the rice blast fungus Pyricularia (Magnaporthe) oryzae, several isolates from the region of origin retain mating ability (female fertility), but most isolates are female sterile. Therefore, it is hypothesized that female fertility was lost during its spread from the origin to the rest of the world, and P. oryzae is an ideal biological model for studying the cause of the evolutionary shift in the reproductive mode. Here, we show that functional mutations of Pro1, a global transcriptional regulator of mating-related genes in filamentous fungi, is one cause of loss of female fertility in this fungus. Employing backcrossing between female-fertile and female-sterile field isolates, we identified the putative genomic region involved in female sterility by comparative genomics between the genomes of F4 female-fertile and -sterile progenies. Further genotyping, linkage, and functional analyses revealed that the functional mutation of Pro1 causes the loss of female fertility. RNA sequencing analysis showed that Pro1 regulates global gene expression, including that of several mating-related genes. The dysfunctional Pro1 did not affect the infection processes, such as conidial germination, appressorium formation, and penetration, but conidial release from conidiophores was increased. Furthermore, various types of mutations in Pro1 were detected in geographically distant P. oryzae, including pandemic isolates of wheat blast fungus. These results provide the first evidence that loss of female fertility may be advantageous to the life cycle of some plant pathogenic fungi. SignificanceMany pathogenic and industrial fungi are thought to have abdicated sexual reproduction, but the mechanisms and biological importance have been a long-standing mystery. Discovering why such fungi lost fertility is important to understand their survival strategies. Here, we revealed the genetic basis of how the rice blast fungus lost female fertility in nature and how this affects the life cycle. This has important implications for understanding evolution of blast pathogens and for developing an effective management strategy to control blast disease before a pandemic. Our findings also provide an additional perspective on advantages of asexual reproduction in some eukaryotes.