The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection

Abstract

Potyviral genomes encode just 11 major proteins and multifunctionality is associated with most of these proteins at different stages of the virus infection cycle. Some potyviral proteins modulate phytohormones and protein degradation pathways and have either pro- or anti-viral/insect vector functions. Our previous work demonstrated that the potyviral protein 6K1 has an antagonistic effect on vectors when expressed transiently in host plants, suggesting plant defenses are regulated. However, to our knowledge the mechanisms of how 6K1 alters plant defenses and how 6K1 functions are regulated are still limited. Here we show that the 6K1 from Turnip mosaic virus (TuMV) reduces the abundance of transcripts related to jasmonic acid biosynthesis and cysteine protease inhibitors when expressed in Nicotiana benthamiana relative to controls. 6K1 stability increased when cysteine protease activity was inhibited chemically, showing a mechanism to the rapid turnover of 6K1 when expressed in trans. Using RNAseq, qRT-PCR, and enzymatic assays, we demonstrate TuMV reprograms plant protein degradation pathways on the transcriptional level and increases 6K1 stability at later stages in the infection process. Moreover, we show 6K1 decreases plant protease activity in infected plants and increases TuMV accumulation in systemic leaves compared to controls. These results suggest 6K1 has a pro-viral function in addition to the anti-insect vector function we observed previously. Although the host targets of 6K1 and the impacts of 6K1-induced changes in protease activity on insect vectors are still unknown, this study enhances our understanding of the complex interactions occurring between plants, potyviruses, and vectors.

Soybean Mosaic Virus 6K1 Interactors Screening and GmPR4 and GmBI1 Function Characterization

“…According to their function description, these proteins were divided into six categories, namely defense-related, transport-related, metabolism-related, DNA binding, unknown, and membrane-related proteins ( Figure 3 ). In this categorization, defense-related proteins accounted for the most (28%), followed by transport-related proteins (20%), suggesting the involvement of 6K1 in viral movement, which is consistent with previous reports [ 29 , 42 ]. This suggestion was further supported by GO analysis, which revealed that candidate genes were significantly enriched in the transport process and transmembrane transporter activity ( Figure 4 A).…”

“…Therefore, the potential interactions found in the Y2H system may not happen during natural infection. However, we have observed the interactions between 6K1 and the Papain family cysteine protease (GmPFCP)/Cysteine protease inhibitors (GmCYSB) that were reported previously [ 42 ], suggesting that the Y2H system is a good system to analyze interaction in vitro. The identification of host factors interacting with 6K1 contributes to the understanding of the molecular mechanism of 6K1 in virus infection.…”

“…In addition, potyviruses infection could alter the phytohormone signal. For example, HC-Pro enhances the expression of defense-related genes in the SA pathway, and 6K1 can inhibit the JA-dependent defenses [ 41 , 42 ]. Exploring the response of host factors to ER stress and phytohormones would facilitate the clarification of the molecular mechanism of host resistance to potyviruses.…”

Foliar Application of Nanoclay Promotes Potato (Solanum tuberosum L.) Growth and Induces Systemic Resistance against Potato Virus Y

“…Moreover, the phytohormones have a significant role in controlling plant–potyvirus and plant–insect interactions. For instance, plants can utilize ethylene (ET), jasmonic acid (JA), and salicylic acid (SA) to fight against a variety of phloem-feeding insects, such as aphids, which are the primary insect carrier for potyviruses [ 54 , 64 , 65 , 66 , 67 ].…”

Potato (Solanum tuberosum L.) Leaf Extract Concentration Affects Performance and Oxidative Stress in Green Peach Aphids (Myzus persicae (Sulzer)

“…The green peach aphid, Myzus persicae (Sulzer), is a major threat to potatoes due to its ability to adapt to a wide range of plant species [ 27 ] and easily develop an anti-insecticide biotype to maintain homeostasis [ 28 ]. In addition to being a significant plant pest, green peach aphids also serve as a vector for potyviruses, resulting in significant production losses [ 29 , 30 ]. When Myzus persicae feeds on the plant epidermis, it transmits potato virus Y, cucumber mosaic virus [ 31 ], and PVY in a non-persistent mode, making management a major concern [ 32 ].…”