Pathogen effectors and plant immunity determine specialization of the blast fungus to rice subspecies

Abstract

Understanding how fungi specialize on their plant host is crucial for developing sustainable disease control. A traditional, centuries-old rice agro-system of the Yuanyang terraces was used as a model to show that virulence effectors of the rice blast fungus Magnaporthe oryzaeh play a key role in its specialization on locally grown indica or japonica local rice subspecies. Our results have indicated that major differences in several components of basal immunity and effector-triggered immunity of the japonica and indica rice varieties are associated with specialization of M. oryzae. These differences thus play a key role in determining M. oryzae host specificity and may limit the spread of the pathogen within the Yuanyang agro-system. Specifically, the AVR-Pia effector has been identified as a possible determinant of the specialization of M. oryzae to local japonica rice.Microbes that cause diseases in plants are a threat to food security. For example, the rice blast fungus Magnaporthe oryzae causes the loss of enough rice to feed 60 million people each year. Disease-causing microbes must overcome the plant’s first line of defense, which includes preformed barriers and antimicrobial responses that are triggered by characteristic molecules found in many different microbes.The microbes that can overcome this first line of defense typically do so with an arsenal of proteins called effectors that interfere with specific biological processes in the plant. To counteract this interference, some plants have evolved genes that encode proteins that detect these effectors and trigger stronger antimicrobial responses. For centuries, farmers and plant breeders have selected for these resistance genes when trying to breed crops that are more resistant to disease. However, over time, disease-causing microbes have lost effectors, which means that several resistance genes have rapidly become ineffective.Some researchers predicted that growing a mixture of varieties of a given crop together might be a better way of protecting crop yields. Over 16 years ago, this idea was proved successful against the rice blast fungus for rice plants grown in China. However, the exact reasons why this strategy worked and its effects on the fungus were not clear.Now Liao, Huang et al. have taken another look at rice varieties grown via the traditional method of terraces of rice paddies in Yuanyang. Some of these varieties had a strong first line of defense and few resistance genes, while others relied much more on resistance genes to protect themselves again the rice blast fungus. Liao, Huang et al. found that growing rice varieties with such different immune systems forces some of the rice blast fungi to accumulate effector proteins to combat the first line of defense, whereas other fungi had to get rid of these effectors to avoid being recognized by the major resistance genes. These two forces led to the evolution of two specialized populations of fungi that can infect specific rice varieties but not others. This means that the fungi cannot spread in the landscape, and so the fields of rice become resistant as a whole.These new findings demonstrate the importance of diversity in rice for sustainable crop protection. The next challenge will be to demonstrate if a similar approach can also protect other major crops grown in different agricultural settings.