Summary: Rice production is threatened by multiple pathogens. Breeding cultivars with broad‐spectrum disease resistance is necessary to maintain and improve crop production. Previously we found that overexpression of miR160a enhanced rice blast disease resistance. However, it is unclear whether miR160a also regulates resistance against other pathogens, and what the downstream signaling pathways are. Here, we demonstrate that miR160a positively regulates broad‐spectrum resistance against the causative agents of blast, leaf blight and sheath blight in rice. Mutations of miR160a‐targeted Auxin Response Factors result in different alteration of resistance conferred by miR160a. miR160a enhances disease resistance partially by suppressing ARF8, as mutation of ARF8 in MIM160 background partially restores the compromised resistance resulting from MIM160. ARF8 protein binds directly to the promoter and suppresses the expression of WRKY45, which acts as a positive regulator of rice immunity. Mutation of WRKY45 compromises the enhanced blast resistance and bacterial leaf blight resistance conferred by arf8 mutant. Overall, our results reveal that a microRNA coordinates rice broad‐spectrum disease resistance by suppressing multiple target genes that play different roles in disease resistance, and uncover a new regulatory pathway mediated by the miR160a‐ARF8 module. These findings provide new resources to potentially improve disease resistance for breeding in rice.

The flower-infecting fungus Ustilaginoidea virens causes rice false smut, which is a severe emerging disease threatening rice (Oryza sativa) production worldwide. False smut not only reduces yield, but more importantly produces toxins on grains, posing a great threat to food safety. U. virens invades spikelets via the gap between the two bracts (lemma and palea) enclosing the floret and specifically infects the stamen and pistil. Molecular mechanisms for the U. virens–rice interaction are largely unknown. Here, we demonstrate that rice flowers predominantly employ chitin-triggered immunity against U. virens in the lemma and palea, rather than in the stamen and pistil. We identify a crucial U. virens virulence factor, named UvGH18.1, which carries glycoside hydrolase activity. Mechanistically, UvGH18.1 functions by binding to and hydrolyzing immune elicitor chitin and interacting with the chitin receptor CHITIN ELICITOR BINDING PROTEIN (OsCEBiP) and co-receptor CHITIN ELICITOR RECEPTOR KINASE1 (OsCERK1) to impair their chitin-induced dimerization, suppressing host immunity exerted at the lemma and palea for gaining access to the stamen and pistil. Conversely, pretreatment on spikelets with chitin induces a defense response in the lemma and palea, promoting resistance against U. virens. Collectively, our data uncover a mechanism for a U. virens virulence factor and the critical location of the host–pathogen interaction in flowers and provide a potential strategy to control rice false smut disease.

Background: Citrus yellow vein-clearing virus (CYVCV) is a Mandarivirus that causes great economic losses in lemon production. CYVCV infection is associated with obvious yellow vein-clearing disease symptoms and is directly regulated by plant hormone responses. Methods: To understand how lemon plants respond to CYVCV infection, we performed transcriptomic and phytohormone metabolomics. Results: A total of 936 differentially expressed genes were identified, and 773 were downregulated. Salicylic acid and auxin levels increased after CYVCV infection, and phytohormone regulatory systems were also explored. Jasmonic acid and auxin levels decreased after the CYVCV challenge, and jasmonic acid and auxin signaling pathway components were mostly downregulated. The differentially expressed genes (DEGs) involved in the immune response to viral infection, including those related to cell wall integrity, lectin, microtubules, and mildew resistance locus O (MLO), may also provide new candidate targets for CYVCV control. Conclusions: Our findings provide new insights into the molecular changes underlying the pathogenesis of CYVCV in lemon plants.