Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection
Pierce’s disease is a major threat to grapevines caused by the bacterium Xylella fastidiosa. Although devoid of a type 3 secretion system commonly employed by bacterial pathogens to deliver effectors inside host cells, this pathogen is able to influence host parenchymal cells from the xylem lumen by...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-06-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2018.00771/full |
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| author | Paulo A. Zaini Rafael Nascimento Hossein Gouran Dario Cantu Sandeep Chakraborty My Phu Luiz R. Goulart Abhaya M. Dandekar |
| author_facet | Paulo A. Zaini Rafael Nascimento Hossein Gouran Dario Cantu Sandeep Chakraborty My Phu Luiz R. Goulart Abhaya M. Dandekar |
| author_sort | Paulo A. Zaini |
| collection | DOAJ |
| description | Pierce’s disease is a major threat to grapevines caused by the bacterium Xylella fastidiosa. Although devoid of a type 3 secretion system commonly employed by bacterial pathogens to deliver effectors inside host cells, this pathogen is able to influence host parenchymal cells from the xylem lumen by secreting a battery of hydrolytic enzymes. Defining the cellular and biochemical changes induced during disease can foster the development of novel therapeutic strategies aimed at reducing the pathogen fitness and increasing plant health. To this end, we investigated the transcriptional, proteomic, and metabolomic responses of diseased Vitis vinifera compared to healthy plants. We found that several antioxidant strategies were induced, including the accumulation of gamma-aminobutyric acid (GABA) and polyamine metabolism, as well as iron and copper chelation, but these were insufficient to protect the plant from chronic oxidative stress and disease symptom development. Notable upregulation of phytoalexins, pathogenesis-related proteins, and various aromatic acid metabolites was part of the host responses observed. Moreover, upregulation of various cell wall modification enzymes followed the proliferation of the pathogen within xylem vessels, consistent with the intensive thickening of vessels’ secondary walls observed by magnetic resonance imaging. By interpreting the molecular profile changes taking place in symptomatic tissues, we report a set of molecular markers that can be further explored to aid in disease detection, breeding for resistance, and developing therapeutics. |
| first_indexed | 2024-12-11T18:22:32Z |
| format | Article |
| id | doaj.art-7738699930834229a0a62e6001cea535 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-11T18:22:32Z |
| publishDate | 2018-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-7738699930834229a0a62e6001cea5352022-12-22T00:55:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-06-01910.3389/fpls.2018.00771364203Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa InfectionPaulo A. Zaini0Rafael Nascimento1Hossein Gouran2Dario Cantu3Sandeep Chakraborty4My Phu5Luiz R. Goulart6Abhaya M. Dandekar7Department of Plant Sciences, University of California, Davis, Davis, CA, United StatesInstitute of Genetics and Biochemistry, Federal University of Uberlândia, Uberlândia, BrazilDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Viticulture and Enology, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesInstitute of Genetics and Biochemistry, Federal University of Uberlândia, Uberlândia, BrazilDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesPierce’s disease is a major threat to grapevines caused by the bacterium Xylella fastidiosa. Although devoid of a type 3 secretion system commonly employed by bacterial pathogens to deliver effectors inside host cells, this pathogen is able to influence host parenchymal cells from the xylem lumen by secreting a battery of hydrolytic enzymes. Defining the cellular and biochemical changes induced during disease can foster the development of novel therapeutic strategies aimed at reducing the pathogen fitness and increasing plant health. To this end, we investigated the transcriptional, proteomic, and metabolomic responses of diseased Vitis vinifera compared to healthy plants. We found that several antioxidant strategies were induced, including the accumulation of gamma-aminobutyric acid (GABA) and polyamine metabolism, as well as iron and copper chelation, but these were insufficient to protect the plant from chronic oxidative stress and disease symptom development. Notable upregulation of phytoalexins, pathogenesis-related proteins, and various aromatic acid metabolites was part of the host responses observed. Moreover, upregulation of various cell wall modification enzymes followed the proliferation of the pathogen within xylem vessels, consistent with the intensive thickening of vessels’ secondary walls observed by magnetic resonance imaging. By interpreting the molecular profile changes taking place in symptomatic tissues, we report a set of molecular markers that can be further explored to aid in disease detection, breeding for resistance, and developing therapeutics.https://www.frontiersin.org/article/10.3389/fpls.2018.00771/fulldefense responseXanthomonadaceaeplant–bacteria interactionvascular pathogentranscriptomeproteome |
| spellingShingle | Paulo A. Zaini Rafael Nascimento Hossein Gouran Dario Cantu Sandeep Chakraborty My Phu Luiz R. Goulart Abhaya M. Dandekar Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection Frontiers in Plant Science defense response Xanthomonadaceae plant–bacteria interaction vascular pathogen transcriptome proteome |
| title | Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection |
| title_full | Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection |
| title_fullStr | Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection |
| title_full_unstemmed | Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection |
| title_short | Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection |
| title_sort | molecular profiling of pierce s disease outlines the response circuitry of vitis vinifera to xylella fastidiosa infection |
| topic | defense response Xanthomonadaceae plant–bacteria interaction vascular pathogen transcriptome proteome |
| url | https://www.frontiersin.org/article/10.3389/fpls.2018.00771/full |
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