Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i>
Mixed virus infections threaten crop production because interactions between the host and the pathogen mix may lead to viral synergism. While individual infections by potato virus A (PVA), a potyvirus, and potato virus X (PVX), a potexvirus, can be mild, co-infection leads to synergistic enhancement...
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-12-01
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| Series: | Viruses |
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| Online Access: | https://www.mdpi.com/1999-4915/15/1/121 |
| _version_ | 1827621337471909888 |
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| author | Maija Pollari Nina Sipari Sylvain Poque Kristiina Himanen Kristiina Mäkinen |
| author_facet | Maija Pollari Nina Sipari Sylvain Poque Kristiina Himanen Kristiina Mäkinen |
| author_sort | Maija Pollari |
| collection | DOAJ |
| description | Mixed virus infections threaten crop production because interactions between the host and the pathogen mix may lead to viral synergism. While individual infections by potato virus A (PVA), a potyvirus, and potato virus X (PVX), a potexvirus, can be mild, co-infection leads to synergistic enhancement of PVX and severe symptoms. We combined image-based phenotyping with metabolite analysis of single and mixed PVA and PVX infections and compared their effects on growth, photosynthesis, and metabolites in <i>Nicotiana benthamiana</i>. Viral synergism was evident in symptom severity and impaired growth in the plants. Indicative of stress, the co-infection increased leaf temperature and decreased photosynthetic parameters. In contrast, singly infected plants sustained photosynthetic activity. The host’s metabolic response differed significantly between single and mixed infections. Over 200 metabolites were differentially regulated in the mixed infection: especially defense-related metabolites and aromatic and branched-chain amino acids increased compared to the control. Changes in the levels of methionine cycle intermediates and a low S-adenosylmethionine/S-adenosylhomocysteine ratio suggested a decline in the methylation potential in co-infected plants. The decreased ratio between reduced glutathione, an important scavenger of reactive oxygen species, and its oxidized form, indicated that severe oxidative stress developed during co-infection. Based on the results, infection-associated oxidative stress is successfully controlled in the single infections but not in the synergistic infection, where activated defense pathways are not sufficient to counter the impact of the infections on plant growth. |
| first_indexed | 2024-03-09T11:02:10Z |
| format | Article |
| id | doaj.art-6733e2eeb1624b648b08c7fbe2e09b25 |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-09T11:02:10Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-6733e2eeb1624b648b08c7fbe2e09b252023-12-01T01:10:32ZengMDPI AGViruses1999-49152022-12-0115112110.3390/v15010121Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i>Maija Pollari0Nina Sipari1Sylvain Poque2Kristiina Himanen3Kristiina Mäkinen4Department of Microbiology, Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, FinlandViikki Metabolomics Unit, Organismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, FinlandDepartment of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, FinlandNational Plant Phenotyping Infrastructure, HiLIFE, Biocenter Finland, Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, FinlandDepartment of Microbiology, Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, FinlandMixed virus infections threaten crop production because interactions between the host and the pathogen mix may lead to viral synergism. While individual infections by potato virus A (PVA), a potyvirus, and potato virus X (PVX), a potexvirus, can be mild, co-infection leads to synergistic enhancement of PVX and severe symptoms. We combined image-based phenotyping with metabolite analysis of single and mixed PVA and PVX infections and compared their effects on growth, photosynthesis, and metabolites in <i>Nicotiana benthamiana</i>. Viral synergism was evident in symptom severity and impaired growth in the plants. Indicative of stress, the co-infection increased leaf temperature and decreased photosynthetic parameters. In contrast, singly infected plants sustained photosynthetic activity. The host’s metabolic response differed significantly between single and mixed infections. Over 200 metabolites were differentially regulated in the mixed infection: especially defense-related metabolites and aromatic and branched-chain amino acids increased compared to the control. Changes in the levels of methionine cycle intermediates and a low S-adenosylmethionine/S-adenosylhomocysteine ratio suggested a decline in the methylation potential in co-infected plants. The decreased ratio between reduced glutathione, an important scavenger of reactive oxygen species, and its oxidized form, indicated that severe oxidative stress developed during co-infection. Based on the results, infection-associated oxidative stress is successfully controlled in the single infections but not in the synergistic infection, where activated defense pathways are not sufficient to counter the impact of the infections on plant growth.https://www.mdpi.com/1999-4915/15/1/121plant-virus interactionsviral synergismmixed infectionphenotypingmetabolite profilingpotyvirus |
| spellingShingle | Maija Pollari Nina Sipari Sylvain Poque Kristiina Himanen Kristiina Mäkinen Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> Viruses plant-virus interactions viral synergism mixed infection phenotyping metabolite profiling potyvirus |
| title | Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> |
| title_full | Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> |
| title_fullStr | Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> |
| title_full_unstemmed | Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> |
| title_short | Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of <i>Nicotiana benthamiana</i> |
| title_sort | effects of poty potexvirus synergism on growth photosynthesis and metabolite status of i nicotiana benthamiana i |
| topic | plant-virus interactions viral synergism mixed infection phenotyping metabolite profiling potyvirus |
| url | https://www.mdpi.com/1999-4915/15/1/121 |
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