NBS-LRR Protein Pik-H4 Interacts with OsBIHD1 to Balance Rice Blast Resistance and Growth by Coordinating Ethylene-Brassinosteroid Pathway

Abstract

The regulation of innate immunity and plant growth, along with the trade-off between them, affects the defense and recovery mechanisms of the plant after it is attacked by pathogens. Although it is known that hormonal crosstalk plays a major role in regulating interaction of plant growth and PAMP-triggered immunity, the relationship between plant growth and effector-triggered immunity (ETI) remains unclear. In a large-scale yeast two-hybrid screening for Pik-H4-interacting proteins, a homeodomain transcription factor OsBIHD1 was identified, which is previously known to function in biotic and abiotic stress responses. The knockout of <i>OsBIHD1</i> in rice lines carrying <i>Pik-H4</i> largely compromised the resistance of the rice lines to <i>Magnaporthe oryzae</i>, the fungus that causes rice blast. While overexpression of <i>OsBIHD1</i> resulted in enhanced expression of the pathogenesis-related (<i>PR</i>) and ethylene (ET) synthesis genes. Moreover, OsBIHD1 was also found to directly bind to the promoter region of ethylene-synthesis enzyme OsACO3. In addition, <i>OsBIHD1</i> overexpression or deficiency provoked dwarfism and reduced brassinosteroid (BR) insensitivity through repressing the expression of several critical genes involved in BR biosynthesis and BR signaling. During <i>M. oryzae</i> infection, transcript levels of the crucial BR catabolic genes (<i>CYP734A2</i>, <i>CYP734A4</i>, and <i>CYP734A6</i>) were significantly up-regulated in <i>OsBIHD1-OX</i> plants. Furthermore, OsBIHD1 was found to be capable of binding to the sequence-specific <i>cis</i>-elements on the promoters of <i>CYP734A2</i> to suppress the plant growth under fungal invasion. Our results collectively suggest a model that OsBIHD1 is required for Pik-H4-mediated blast resistance through modulating the trade-off between resistance and growth by coordinating brassinosteroid-ethylene pathway.