Nonhost resistance and effectors in interactions between Colletotrichum species and plants

Abstract

Pathogenic microbial species generally colonize a limited number of plant species, i.e., they display clear host specificity, mainly because plant species outside of the host range mount nonhost resistance against infection trials by nonadapted pathogens. For the establishment of ‘basic compatibility’ with host plant species, fungal plant pathogens are inferred to utilize virulence factors, including secreted effector proteins, to suppress nonhost resistance. But how virulence effectors contribute to fungal host range remains elusive. The fungal genus Colletotrichum causes anthracnose disease in a wide variety of plants including numerous economically important crops. Our group is continuously studying nonhost plant resistance against Colletotrichum fungi and is also focusing on the relation of Colletotrichum effectors with host specificity. In Arabidopsis thaliana, PEN2 and EDR1 are involved in preinvasive nonhost resistance against nonadapted pathogen C. tropicale. If the pathogen invades the mutants defective in preinvasive resistance such as the pen2 mutants, postinvasive resistance is newly activated, which terminates further fungal expansion. The findings suggest nonhost plant resistance against Colletotrichum fungi depends on the multilayered defense system, which guarantees robustness in nonhost resistance, although adapted pathogens clearly suppress this robust resistance via unknown ways. Colletotrichum orbiculare infects cucurbitaceous crops such as cucumber, watermelon, and melon. C. orbiculare also can infect Nicotiana benthamiana, a distantly related Solanaceae species. We revealed that the effector NIS1 of C. orbiculare, highly conserved in a wide range of fungal pathogens, interacts with the pattern recognition receptor-associated kinases BAK1 and BIK1, thereby inhibiting their function. However, the knockout analysis of the NIS1 gene revealed that NIS1 is not essential for virulence of C. orbiculare. Through targeted gene knockout screening of C. orbiculare ‘core’ effector candidates defined based on in planta gene expression, we recently identified four virulence effectors, named EPC1 to EPC4, that are required for full virulence of C. orbiculare to cucurbitaceous cultivars, but not to the Solanaceae plant N. benthamiana. The finding suggests that the identified effectors are involved in host specificity of C. orbiculare on the cucurbitaceous plants.