Turnip mosaic virus P1 suppresses JA biosynthesis by degrading cpSRP54 that delivers AOCs onto the thylakoid membrane to facilitate viral infection

Abstract

Jasmonic acid (JA) is a crucial hormone in plant antiviral immunity. Increasing evidence shows that viruses counter this host immune response by interfering with JA biosynthesis and signaling. However, the mechanism by which viruses affect JA biosynthesis is still largely unexplored. Here, we show that a highly conserved chloroplast protein cpSRP54 was downregulated in Nicotiana benthamiana infected by turnip mosaic virus (TuMV). Its silencing facilitated TuMV infection. Furthermore, cpSRP54 interacted with allene oxide cyclases (AOCs), key JA biosynthesis enzymes, and was responsible for delivering AOCs onto the thylakoid membrane (TM). Interestingly, TuMV P1 protein interacted with cpSRP54 and mediated its degradation via the 26S proteosome and autophagy pathways. The results suggest that TuMV has evolved a strategy, through the inhibition of cpSRP54 and its delivery of AOCs to the TM, to suppress JA biosynthesis and enhance viral infection. Interaction between cpSRP54 and AOCs was shown to be conserved in Arabidopsis and rice, while cpSRP54 also interacted with, and was degraded by, pepper mild mosaic virus (PMMoV) 126 kDa protein and potato virus X (PVX) p25 protein, indicating that suppression of cpSRP54 may be a common mechanism used by viruses to counter the antiviral JA pathway.

Pepper mild mottle virus coat protein interacts with pepper chloroplast outer envelope membrane protein OMP24 to inhibit antiviral immunity in plants

“…TuMV Vpg impairs the antiviral PCC induced by NbNdhM [ 58 ]. TuMV P1 interacts with chloroplast protein cpSRP54 to suppress JA-mediated resistance [ 33 ]. Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses by interfering with interactions between NTRC and 2-Cys Prx [53] .…”

Geminivirus C4 proteins inhibit GA signaling via prevention of NbGAI degradation, to promote viral infection and symptom development in N. benthamiana

“…Rice black-streaked dwarf virus (RBSDV)-encoded P5-1 can regulate the ubiquitination activity of SCF E3 ligases and inhibit the jasmonate signaling pathway to benefit its infection in rice [ 52 ]. Turnip mosaic virus (TuMV) P1 protein interacts with cpSRP54 and mediates its degradation via the 26S proteosome and autophagy pathways, thereby inhibiting the cpSRP54-facilitated delivery of AOCs to the thylakoid membrane and manipulation of JA-mediated defense [ 53 ]. Tobacco mosaic virus (TMV) replication-associated protein has been demonstrated to affect the localization and stability of auxin/indole-3-acetic acid (IAA) proteins in Arabidopsis to promote its infection [ 54 , 55 ].…”

Small Talk: On the Possible Role of Trans-Kingdom Small RNAs during Plant–Virus–Vector Tritrophic Communication

“…Viruses do not only counterdefend against antiviral RNAi by direct interference at major steps of the RNAi pathway via viral suppressor proteins of RNAi (VSRs), topics that have been extensively reviewed in the past decade [ 15 , 28 , 88 ]. They are also able to dampen the Ca 2+ -induced, and further downstream, JA-mediated defense responses via the very same VSRs or other viral proteins [ 89 , 90 , 91 , 92 , 93 ], and as a result often enhance viral infection and modulate vector behavior/performance. For example, geminivirus V2 protein disrupts CAMTA3-calmodulin interactions [ 87 ].…”