Rice black‐streaked dwarf virus‐encoded P5‐1 regulates the ubiquitination activity of SCF E3 ligases and inhibits jasmonate signaling to benefit its infection in rice

Abstract

SCF (Skp1/Cullin1/F-box) complexes are key regulators of many cellular processes. Viruses encode specific factors to interfere with or hijack these complexes and ensure their infection in plants. The molecular mechanisms controlling this interference/hijack are currently largely unknown. Here, we present evidence of a novel strategy used by Rice black-streaked dwarf virus (RBSDV) to regulate ubiquitination in rice (Oryza sativa) by interfering in the activity of OsCSN5A. We also show that RBSDV P5-1 specifically affects CSN-mediated deRUBylation of OsCUL1, compromising the integrity of the SCF COI1 complex. We demonstrate that the expressions of jasmonate (JA) biosynthesis-associated genes are not inhibited, whereas the expressions of JA-responsive genes are down-regulated in transgenic P5-1 plants. More importantly, application of JA to P5-1 transgenic plants did not reduce their susceptibility to RBSDV infection. Our results suggest that P5-1 inhibits the ubiquitination activity of SCF E3 ligases through an interaction with OsCSN5A, and hinders the RUBylation/deRUBylation of CUL1, leading to an inhibition of the JA response pathway and an enhancement of RBSDV infection in rice.

Alterations of Rice (Oryza sativa L.) DNA Methylation Patterns Associated with Gene Expression in Response to Rice Black Streaked Dwarf Virus

“…Previous studies on rice plants defense against RBSDV mainly focused on RNAi [ 21 , 22 ] and plant hormone signaling pathways [ 23 ]. For instance, the jasmonate (JA) and auxin signaling pathways enhance plant defense against RBSDV [ 24 , 25 ], whereas brassinosteroid (BR) and abscicic acid (ABA) pathways facilitated the viral infection [ 25 , 26 ]. However, the role of host DNA methylation in RBSDV infection still remains unclear.…”

Comparative Proteomic Analysis of Nicotiana Benthamiana Seedings Under Chinese Wheat Mosaic Virus Infection

“…Western blot assay was performed as described previously with small modifications [6,31]. Collected samples were individually ground in liquid nitrogen and then homogenized in a protein extraction buffer (Sigma-Aldrich, St. Louis, MO, USA) supplemented with Protease Inhibitor Cocktail Tablets (Roche, 1 tablet/50mL buffer).…”

“…For instance, rice dwarf virus (RDV) infection subverts auxin signaling in rice as the interaction between RDV P2 protein and OsIAA10 disrupts the interaction of OsIAA10 and OsTIR1 [5]. Rice black streak dwarf virus (RBSDV) encoded P5-1 protein physically interacts with OsCSN5A, which interferes with the ubiquitination activity of SCF E3 ligase and suppress jasmonate signaling to benefit viral infection in rice [6].…”

Systematic Identification and Functional Analysis of Circular RNAs During Rice Black-Streaked Dwarf Virus Infection in the Laodelphax striatellus (Fallén) Midgut

“…RBSDV is transmitted in a persistent propagative manner by Laodelphax striatellus (Fallén) (Wu et al, 2020). The genome of RBSDV contains 10 double-stranded RNA (dsRNA) segments (S1 to S10) and encodes 13 proteins (Milne et al, 1973;Zhang et al, 2001a;He et al, 2020). Most RBSDV genomic segments encode one protein, while S5, S7, and S9 encode two proteins.…”

“…Most RBSDV genomic segments encode one protein, while S5, S7, and S9 encode two proteins. P5-1, P6, and P9-1 proteins encoded by S5, S6, and S9 are the components of the viroplasm (Li et al, 2013;Sun et al, 2013;He et al, 2020). The P10 protein, encoded by S10, is the virus outer capsid protein.…”