Suppression of Jasmonic Acid-Mediated Defense by Viral-Inducible MicroRNA319 Facilitates Virus Infection in Rice

Abstract

MicroRNAs (miRNAs) are pivotal modulators of plant development and host-virus interactions. However, the roles and action modes of specific miRNAs involved in viral infection and host susceptibility remain largely unclear. In this study, we show that Rice ragged stunt virus (RRSV) infection caused increased accumulation of miR319 but decreased expression of miR319-regulated TCP (TEOSINTE BRANCHED/CYCLOIDEA/PCF) genes, especially TCP21, in rice plants. Transgenic rice plants overexpressing miR319 or downregulating TCP21 exhibited disease-like phenotypes and showed significantly higher susceptibility to RRSV in comparison with the wild-type plants. In contrast, only mild disease symptoms were observed in RRSV-infected lines overexpressing TCP21 and especially in the transgenic plants overexpressing miR319-resistant TCP21. Both RRSV infection and overexpression of miR319 caused the decreased endogenous jasmonic acid (JA) levels along with downregulated expression of JA biosynthesis and signaling-related genes in rice. However, treatment of rice plants with methyl jasmonate alleviated disease symptoms caused by RRSV and reduced virus accumulation. Taken together, our results suggest that the induction of miR319 by RRSV infection in rice suppresses JA-mediated defense to facilitate virus infection and symptom development.

Magnaporthe oryzae Induces the Expression of a MicroRNA to Suppress the Immune Response in Rice

“…By 227 contrast, OsTCP21 function is related to rice responses to biotic and abiotic stresses. For 228 example, OsTCP21 is involved in synthesis and signaling of JA in response to cold stress and 229 virus infection (Wang, Sun et al 2014, Zhang, Ding et al 2016. Therefore, we concentrated 230 our study on the miR319/OsTCP21 regulatory module in rice defense responses against the 231 blast disease.…”

“…Therefore, we concentrated 230 our study on the miR319/OsTCP21 regulatory module in rice defense responses against the 231 blast disease. 232 233 miR319b overexpression causes rice susceptibility to the blast disease 234 To investigate the involvement of miR319 in rice immunity against the blast disease, we 235 employed a miR319b-overexpression line (miR319b-OE) and an OsTCP21 mutant line 236 (OsTCP21-Res) in which the OsTCP21 gene is relieved from regulation by miR319b due to 237 engineered synonymous mismatches (Zhang, Ding et al 2016). When disease responses 238 against Guy11 infection were compared among wild-type, miR319b-OE, and OsTCP21-Res 239 rice, miR319b-OE showed obviously stronger disease symptoms than the wild-type rice, such 240 as heavily developed lesions, obvious chlorosis ( Figure 3A), and significantly more hyphae 241 accumulation (biomass) ( Figure 3B).…”

“…The JA signaling pathway is a potent mechanism 439 employed by plants that can defend against necrotrophic and hemibiotrophic pathogens, 440 including the blast pathogen (Thaler, Humphrey et al 2012, Tamaoki, Seo et al 2013 Ding et al 2016). In tomato, miR319 behaves as a systemic signal and a negative regulator of 442 defense responses against RKN through decreasing the JA level (Zhao, Li et al 2015 (Zhang, Ding et al 2016). In our study, JA signaling was induced at the early 446 stage but declined at the late stage (Supplemental Figure S2), which matched the expression 447 pattern of miR319 very well ( Figure 1C).…”

“…In tomato, sl-miR319 behaves both as a 122 systemic signal and a regulatory factor of defense response to root-knot nematodes (RKN) 123 . 124 The jasmonic acid (JA) signaling pathway is a key regulator of plant defense response 125 against both hemibiotrophic and necrotrophic pathogens (Thaler et al 2012, Tamaoki et al 126 2013, Zhang et al 2016). Ath-miR319 regulates the expression of a key JA synthetic 127 component, LIPOXYGENASE 2 (LOX2), through silencing TCP4 and TCP20 (Schommer et 128 al.…”

“…2008, Danisman et al 2012. In rice infected by Rice Ragged Stunt Virus (RRSV), induced 129 expression of miR319 is associated with promoted viral infection, suppression of OsTCP21, 130 down-regulation of JA synthetic genes, and reduced JA accumulation, indicating that RRSV 131 may manipulate endogenous JA levels through miR319 (Zhang, Ding et al 2016). Therefore,132 it is suggested that miR319/TCP may manipulate plant innate response against RRSV by 133 affecting JA synthesis and signaling.…”