The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection
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 function...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-06-01
|
| Series: | Viruses |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1999-4915/14/6/1341 |
| _version_ | 1827655749099061248 |
|---|---|
| author | Sayanta Bera Gabriella D. Arena Swayamjit Ray Sydney Flannigan Clare L. Casteel |
| author_facet | Sayanta Bera Gabriella D. Arena Swayamjit Ray Sydney Flannigan Clare L. Casteel |
| author_sort | Sayanta Bera |
| collection | DOAJ |
| description | 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 <i>Turnip mosaic virus</i> (TuMV) reduces the abundance of transcripts related to jasmonic acid biosynthesis and cysteine protease inhibitors when expressed in <i>Nicotiana benthamiana</i> 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 <i>trans</i>. 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. |
| first_indexed | 2024-03-09T22:12:59Z |
| format | Article |
| id | doaj.art-1e6f397beead473c883a8b81ccc451f2 |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-09T22:12:59Z |
| publishDate | 2022-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-1e6f397beead473c883a8b81ccc451f22023-11-23T19:27:48ZengMDPI AGViruses1999-49152022-06-01146134110.3390/v14061341The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> InfectionSayanta Bera0Gabriella D. Arena1Swayamjit Ray2Sydney Flannigan3Clare L. Casteel4School of Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, NY 14850, USALaboratório de Biologia Molecular Aplicada, Instituto Biológico de São Paulo, São Paulo 04014-002, BrazilSchool of Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, NY 14850, USASchool of Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, NY 14850, USASchool of Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, NY 14850, USAPotyviral 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 <i>Turnip mosaic virus</i> (TuMV) reduces the abundance of transcripts related to jasmonic acid biosynthesis and cysteine protease inhibitors when expressed in <i>Nicotiana benthamiana</i> 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 <i>trans</i>. 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.https://www.mdpi.com/1999-4915/14/6/1341<i>Arabidopsis thaliana</i>defencejasmonic acidMPMIpapain-like cysteine proteasesphytohormones |
| spellingShingle | Sayanta Bera Gabriella D. Arena Swayamjit Ray Sydney Flannigan Clare L. Casteel The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection Viruses <i>Arabidopsis thaliana</i> defence jasmonic acid MPMI papain-like cysteine proteases phytohormones |
| title | The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection |
| title_full | The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection |
| title_fullStr | The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection |
| title_full_unstemmed | The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection |
| title_short | The Potyviral Protein 6K1 Reduces Plant Proteases Activity during <i>Turnip mosaic virus</i> Infection |
| title_sort | potyviral protein 6k1 reduces plant proteases activity during i turnip mosaic virus i infection |
| topic | <i>Arabidopsis thaliana</i> defence jasmonic acid MPMI papain-like cysteine proteases phytohormones |
| url | https://www.mdpi.com/1999-4915/14/6/1341 |
| work_keys_str_mv | AT sayantabera thepotyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT gabrielladarena thepotyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT swayamjitray thepotyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT sydneyflannigan thepotyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT clarelcasteel thepotyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT sayantabera potyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT gabrielladarena potyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT swayamjitray potyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT sydneyflannigan potyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection AT clarelcasteel potyviralprotein6k1reducesplantproteasesactivityduringiturnipmosaicvirusiinfection |