Pro1 protein malfunction allows rice blast fungus to thrive, new study shows

The ‘paradox of sex’ refers to the puzzle of why the sexual mode of reproduction is more common among living beings than the asexual mode. Sexual reproduction requires at least two mates, exposes individuals to a higher risk of diseases, and is more energy intensive. In contrast, asexual reproduction makes up for all of these disadvantages by requiring only one parent while allowing for the rapid generation of offspring. Now, this ‘paradox’ has been bolstered by findings from a new study regarding a species of pathogenic fungi that infects a variety of cultivates grains, such as rice, wheat, barley, and finger millet.

Pyricularia (Magnaporthe) oryzae, a species of pathogenic filamentous fungi, wreaks havoc on global rice production as it causes the rice blast disease, which has earned it the moniker ‘rice blast fungus’. The infection cycle begins with asexual reproduction, where asexual spores called ‘conidia’ attach to the surface of the leaves of the rice plant. This produces an infection-specific structure called an appressorium, which starts to penetrate the outermost cell layer of the leaf, resulting in visible lesions on the leaf surface. When conditions are favorable, specialized structures called conidiophores emerge and produce more conidia, which disperse through the wind or atmospheric droplets to more rice plants.

While this asexual mode of reproduction is the main driving force of the P. oryzae life cycle, scientists have demonstrated the successful sexual reproduction of this fungus in laboratory settings. The fungus appears to have strains equivalent to biological males and biological females. However, most specimens collected from the fields show a loss of female fertility. The underlying genes and mechanisms responsible for the loss of sexual reproduction in P. oryzae have remained a mystery.

Researchers from the Tokyo University of Science, the National Agriculture and Food Research Organization, and the Tokyo University of Agriculture and Technology, Japan, have recently uncovered evidence for this advantageous loss of sexual reproduction in the rice blast fungus. The research team was led by Professor Takashi Kamakura and Junior Associate Professor Takayuki Arazoe, from the Department of Applied Biological Science at the Tokyo University of Science. Their study was made available online on June 13, 2023, and was published in Volume 26 Issue 27 of the journal iScience on July 21, 2023.

Regarding the premise of the study Prof. Kamakura explains, “Many fungal species have abandoned sexual reproduction, which doesn’t align with the evolutionary advantages of sex and fuels the paradox of sex. In the future, this research will also help breed useful industrial strains or understand how pathogens respond to mutations by explaining how diversity is acquired in fungi.”

The researchers used multiple genetic experiments to identify which genes were linked to female sterility. Parental strains from P. oryzae field isolates were bred to give rise to female-sterile and female-fertile P. oryzae offspring.

Further genetic analyses revealed that mutations that resulted in dysfunctional Pro1 protein (involved in the expression of mating-related genes in filamentous fungi) caused female sterility in rice blast fungus. Dr. Arazoe further exclaims and adds, “To our surprise, the dysfunctional Pro1 increased the release of conidia but did not affect P. oryzae’s pathogenicity. We also found Pro1 mutations in wheat-infecting isolates, which is feared to spread worldwide (pandemic)—a finding that suggests a similar evolution (loss of sexual reproduction) has  occurred in wheat blast fungus.” Building on these results, the research group is already spearheading the identification and characterization of other genes that cause female sterility in fungal species.

Explaining the broader implications of this work, Prof. Kamakura concludes, “We’ve provided the first evidence that the loss of female fertility may be an adaptive advantage for this plant pathogen. The release of asexual conidia favors dispersal in the wild. This work also opens doors to study how diversity, another important aspect of fitness, is acquired in asexual breeders.”   

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Reference

DOI: https://doi.org/10.1016/j.isci. 2023.107020

About The Tokyo University of Science
Tokyo University of Science (TUS) is a well-known and respected university, and the largest science-specialized private research university in Japan, with four campuses in central Tokyo and its suburbs and in Hokkaido. Established in 1881, the university has continually contributed to Japan's development in science through inculcating the love for science in researchers, technicians, and educators.

With a mission of “Creating science and technology for the harmonious development of nature, human beings, and society", TUS has undertaken a wide range of research from basic to applied science. TUS has embraced a multidisciplinary approach to research and undertaken intensive study in some of today's most vital fields. TUS is a meritocracy where the best in science is recognized and nurtured. It is the only private university in Japan that has produced a Nobel Prize winner and the only private university in Asia to produce Nobel Prize winners within the natural sciences field.

Website: https://www.tus.ac.jp/en/mediarelations/

About Professor Takashi Kamakura from Tokyo University of Science
Takashi Kamakura is a Professor in the Department of Applied Biological Science, Faculty of Science and Technology at Tokyo University of Science. His research aims to explain the fundamental biological phenomena seen in fungi that remain unexplained, and he is also interested in answering questions on how fungi acquired these unique abilities. His research themes span fungal differentiation-related genes, fungal gene regulation, and the effects various drugs have on fungi. He has published over 55 peer-reviewed articles since 1987.

Funding information
Funds from a Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Young Scientists (A) (17H05021) and a JSPS Grant-in-Aid for Scientific Research (C) (22K05658) supported the work.