Rice siR109944 suppresses plant immunity to sheath blight and impacts multiple agronomic traits by affecting auxin homeostasis

Abstract

Plant small RNAs (sRNAs) play significant roles in regulating various developmental processes and hormone signalling pathways involved in plant responses to a wide range of biotic and abiotic stresses. However, the functions of sRNAs in response to rice sheath blight remain unclear. We screened rice (Oryza sativa) sRNA expression patterns against Rhizoctonia solani and found that Tourist-miniature inverted-repeat transposable element (MITE)-derived small interfering RNA (siRNA) (here referred to as siR109944) expression was clearly suppressed upon R. solani infection. One potential target of siR109944 is the F-Box domain and LRRcontaining protein 55 (FBL55), which encode the transport inhibitor response 1 (TIR1)-like protein. We found that rice had significantly enhanced susceptibility when siR109944 was overexpressed, while FBL55 OE plants showed resistance to R. solani challenge. Additionally, multiple agronomic traits of rice, including root length and flag leaf inclination, were affected by siR109944 expression. Auxin metabolism-related and signalling pathway-related genes were differentially expressed in the siR109944 OE and FBL55 OE plants. Importantly, pre-treatment with auxin enhanced sheath blight resistance by affecting endogenous auxin homeostasis in rice. Furthermore, transgenic Arabidopsis overexpressing siR109944 exhibited early flowering, increased tiller numbers, and increased susceptibility to R. solani. Our results demonstrate that siR109944 has a conserved function in interfering with plant immunity, growth, and development by affecting auxin homeostasis in planta. Thus, siR109944 provides a genetic target for plant breeding in the future. Furthermore, exogenous application of indole-3-acetic acid (IAA) or auxin analogues might effectively protect field crops against diseases.

Strategies to Manage Rice Sheath Blight: Lessons from Interactions between Rice and Rhizoctonia solani

“…Consistently, mutation of G-protein γ subunit DEP1 can promote rice resistance to RSB (Liu et al 2020;Sun et al 2019;Sun et al 2020a). Furthermore, auxin application enhances rice resistance to sheath blight (Qiao et al 2020;Sun et al 2019). These results indicate that auxin signaling positively regulates RSB resistance and that application of auxin analogues might effectively protect field crops against the disease.…”

“…The small RNA targets F-Box domain-and LRR-containing protein 55 (FBL55) encoding transport inhibitor response 1 (TIR1)-like protein. The siR109944-overexpressing rice plants have a significantly enhanced susceptibility to R. solani, while FBL55-overexpression causes the transgenic plants to be more resistant to RSB (Qiao et al 2020). Additionally, multiple indeterminate domain (IDD) proteins including LPA1 (Loose Plant Architecture 1), IDD3 and IDD13 form a transcription factor complex and regulate expression of the auxin efflux carrier gene PIN-FORMED 1a (PIN1a) in rice through binding to its promoter (Sun et al 2019;Sun et al 2020a).…”

Contribution of Small RNA Pathway to Interactions of Rice with Pathogens and Insect Pests

“…Overexpression of siR109944 facilitates the growth of R. solani companying with reduced IAA accumulation, whereas overexpression of OsFBL55 significantly suppresses R. solani growth associating with increased IAA accumulation. Consistently, IAA application improves resistance to R. solani, suggesting that IAA positively regulates rice sheath blight resistance and siR109944 manipulates auxin signal pathway to negatively regulate rice resistance to R. solani (Qiao et al 2020). Furthermore, sRNAs derived from R. solani are also found to be involved in rice-R. solani interaction.…”

“…Moreover, 14 long siRNAs (lsiRNAs) in length from 25-to 30-nt and several sRNAs are also identified to be responsive to R. sonali. Among them, some siRNAs-target modules show a tight conversely co-expression relationship, including lsiRNA51031-Os08g15322, lsiRNA73750-Os09g14490, lsiRNA118183-Os08g06220, lsiRNA194568-Os06g38990, miR167h-OsARF8, miR171a-Os02g44360, and miR160c-OsARF10, suggesting their involvement in regulating rice response to R. solani (Niu et al 2018;Qiao et al 2020). Among these differentially expressed sRNAs, siR109944 is further proved as a negative regulator in rice resistance against R. solani.…”

Expression of rice siR109944 in Arabidopsis affects plant immunity to multiple fungal pathogens

“…[5][6][7] Based on our present study, we found that rice Touristminiature inverted-repeat transposable element (MITE)derived siR109944 suppressed plant immunity to sheath blight, and overexpression of siR109944 in Arabidopsis could enhance susceptibility to Rhizoctonia solani by modulating auxin homeostasis. 8 To explore whether overexpression of siR109944 enhanced the broad-spectrum immune response in Arabidopsis, the OE line with a higher expression level was selected for this study. 8 We first inoculated siR109944 OE and Col-0 WT seedlings with B. cinerea, a destructive fungus.…”