IDENTIFICATION OF COMMON MECHANISMS TO INTRACELLULARLY ACCOMMODATE BENEFICIAL OR PATHOGENIC FUNGI IN RICE
Rice is a vital cereal crop that feeds over half of the world's population, making it crucial to explore mechanisms that enhance yield or reduce losses. Arbuscular mycorrhizal (AM) fungi such as Rhizophagus irregularis act as beneficial symbionts that enhance plant growth by facilitating nutrient uptake from the soil. In contrast, Magnaporthe oryzae causes rice blast disease, which significantly reduces annual rice yields. Despite their opposing roles, their respective colonization of rice roots share similarities at the transcriptional and morphological level in host cells. This study investigates potential common genetic mechanisms for the intracellular accommodation of these fungi in rice roots. The functional roles of genes commonly induced during both R. irregularis and M. oryzae root colonization were examined to determine if they are part of a shared plant genetic mechanism that promotes the accommodation of these fungi in rice roots, specifically three genes encoding an Exo70 exocyst component, a L-type lectin receptor-like kinase (LecRLK), and a Domain of Unknown Function 538 (DUF538) protein, respectively. While none of these genes were found to be directly essential for the intracellular accommodation of either fungus, a novel role for OsLecRLK in initiating AM symbiosis was suggested, evidenced by a penetration defect observed in oslecrlk mutants. Although LecRLKs have previously been implicated in microbial perception during symbiosis and pathogenesis, this research is the first to propose a role for a LecRLK in establishing symbiosis in rice. Furthermore, the study uncovered common spatiotemporal patterns in the promoter activity of a DUF538 gene during both R. irregularis and M. oryzae root colonization, suggesting that it may be part of a shared host accommodation program. Microbe recognition in plants is mediated by the detection of microbe-associated molecular patterns (MAMPs) by plasma membrane-bound receptors, which then activate cellular signalling pathways, leading to either immune responses or symbiosis. A key conceptual advance of this study is the identification of rice Chitin Elicitor Receptor Kinase 1 (CERK1) as a shared signalling component facilitating root colonization by both symbiotic and pathogenic fungi. This finding challenges the conventional perception of CERK1 as an immune receptor in pathogenic interactions, instead revealing it as a shared signalling component that facilitates the root colonization of both symbiotic R. irregularis and pathogenic M. oryzae in rice. The rice Chitin Elicitor Binding Protein (CEBiP), traditionally recognized for forming a receptor complex with CERK1 to mediate chitin-triggered immunity against fungal pathogens like M. oryzae in foliar infections, has now been identified as a positive regulator of M. oryzae root infection. The findings underscore the complex, organ- specific roles of CERK1 and CEBiP, which exhibit opposing functions depending on whether they are in leaves or roots. Additionally, this research highlights the lifestyle of the fungi as a potential factor influencing these contrasting roles of these receptors in different plant organs. Furthermore, this study proposes that in rice, CERK1 and Nod Factor Receptor 5 (NFR5), which has been implicated in the initiation of symbiosis signalling, may collaborate during the early stages of M. oryzae root colonization. While the formation of a CERK1- NFR5 complex was previously suggested for AM symbiosis, our research extends this concept, proposing that these receptors may also function together to facilitate pathogenic M. oryzae colonization in rice roots. This work provides a new conceptual framework for understanding how plants balance symbiotic and pathogenic interactions. By elucidating the dual roles of key receptors and shared genetic mechanisms in managing diverse microbial interactions, this research contributes to our understanding of plant-microbe relationships and offers new perspectives for improving crop resilience and productivity.
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