Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism
Phytophthora root rot caused by the hemibiotrophic oomycete, Phytophthora cinnamomi is a major biotic hindrance in meeting the ever-increasing demand for avocados. In addition, the pathogen is a global menace to agriculture, horticulture and forestry. Phosphite trunk injections and foliar sprays rem...
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Frontiers Media S.A.
2025-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1632726/full |
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| author | S. Ashok Prabhu S. Ashok Prabhu Previn Naicker Tuan A. Duong Ireshyn Selvan Govender Juanita Engelbrecht Juanita Engelbrecht Robert Backer Robert Backer Stoyan Hristov Stoychev Noëlani van den Berg Noëlani van den Berg |
| author_facet | S. Ashok Prabhu S. Ashok Prabhu Previn Naicker Tuan A. Duong Ireshyn Selvan Govender Juanita Engelbrecht Juanita Engelbrecht Robert Backer Robert Backer Stoyan Hristov Stoychev Noëlani van den Berg Noëlani van den Berg |
| author_sort | S. Ashok Prabhu |
| collection | DOAJ |
| description | Phytophthora root rot caused by the hemibiotrophic oomycete, Phytophthora cinnamomi is a major biotic hindrance in meeting the ever-increasing demand for avocados. In addition, the pathogen is a global menace to agriculture, horticulture and forestry. Phosphite trunk injections and foliar sprays remain the most effective chemical management strategy used in commercial avocado orchards against the pathogen. Phosphite is known to counter P. cinnamomi both directly and indirectly through fortification of host defense. However, phosphite's direct mode of action is still not understood completely. This study identified a P. cinnamomi isolate GKB4 sensitive to phosphite (EC50 of 27.9 μg/mL) and investigated the direct impact of phosphite on this isolate through label-free quantitative SWATH-MS. Proteomics data analysis of untreated vs. phosphite-treated samples revealed that the xenobiotic affects the pathogen's growth by targeting the oxidoreductases whose abundance is significantly reduced. Further, perturbations in the energy metabolism and membrane/transmembrane proteins and transporters, and oxidative stress contribute to growth inhibition. The current study also identified increased putrescine biosynthesis, a polyamine, that when present at non-optimal concentrations could be cytostatic/cytotoxic. The differential expression of enzymes involved in the biosynthesis of secondary metabolites and the intermediates/precursors involved in their biosynthesis is an interesting finding that needs further investigation to ascertain their role in phosphite-induced stress. The pathogen's attempt to counter phosphite's growth-inhibitory effects—through upregulation of alternate bioenergetics pathways (amino acid catabolism and β-oxidation of fatty acids), mitochondrial translation and translocation machinery, peroxisomal proteins, and antioxidants—appears ineffective. This research furthers our limited understanding of the direct in vitro effects of phosphite on P. cinnamomi and has identified potential candidates for molecular functional investigation. |
| format | Article |
| id | doaj-art-d627d8f258b64da1ac4e596750cdb6e0 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-d627d8f258b64da1ac4e596750cdb6e02025-08-25T05:25:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-08-011610.3389/fmicb.2025.16327261632726Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolismS. Ashok Prabhu0S. Ashok Prabhu1Previn Naicker2Tuan A. Duong3Ireshyn Selvan Govender4Juanita Engelbrecht5Juanita Engelbrecht6Robert Backer7Robert Backer8Stoyan Hristov Stoychev9Noëlani van den Berg10Noëlani van den Berg11Hans Merensky Chair in Avocado Research, University of Pretoria, Pretoria, South AfricaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaReSyn Biosciences, Edenvale, South AfricaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaFuture Production Chemicals, Council for Scientific and Industrial Research, Pretoria, South AfricaHans Merensky Chair in Avocado Research, University of Pretoria, Pretoria, South AfricaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaHans Merensky Chair in Avocado Research, University of Pretoria, Pretoria, South AfricaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaEvosep Aps, Odense, DenmarkHans Merensky Chair in Avocado Research, University of Pretoria, Pretoria, South AfricaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaPhytophthora root rot caused by the hemibiotrophic oomycete, Phytophthora cinnamomi is a major biotic hindrance in meeting the ever-increasing demand for avocados. In addition, the pathogen is a global menace to agriculture, horticulture and forestry. Phosphite trunk injections and foliar sprays remain the most effective chemical management strategy used in commercial avocado orchards against the pathogen. Phosphite is known to counter P. cinnamomi both directly and indirectly through fortification of host defense. However, phosphite's direct mode of action is still not understood completely. This study identified a P. cinnamomi isolate GKB4 sensitive to phosphite (EC50 of 27.9 μg/mL) and investigated the direct impact of phosphite on this isolate through label-free quantitative SWATH-MS. Proteomics data analysis of untreated vs. phosphite-treated samples revealed that the xenobiotic affects the pathogen's growth by targeting the oxidoreductases whose abundance is significantly reduced. Further, perturbations in the energy metabolism and membrane/transmembrane proteins and transporters, and oxidative stress contribute to growth inhibition. The current study also identified increased putrescine biosynthesis, a polyamine, that when present at non-optimal concentrations could be cytostatic/cytotoxic. The differential expression of enzymes involved in the biosynthesis of secondary metabolites and the intermediates/precursors involved in their biosynthesis is an interesting finding that needs further investigation to ascertain their role in phosphite-induced stress. The pathogen's attempt to counter phosphite's growth-inhibitory effects—through upregulation of alternate bioenergetics pathways (amino acid catabolism and β-oxidation of fatty acids), mitochondrial translation and translocation machinery, peroxisomal proteins, and antioxidants—appears ineffective. This research furthers our limited understanding of the direct in vitro effects of phosphite on P. cinnamomi and has identified potential candidates for molecular functional investigation.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1632726/fullSWATH-MSphosphitePhytophthora cinnamomioxidoreductasesmetabolismantioxidants |
| spellingShingle | S. Ashok Prabhu S. Ashok Prabhu Previn Naicker Tuan A. Duong Ireshyn Selvan Govender Juanita Engelbrecht Juanita Engelbrecht Robert Backer Robert Backer Stoyan Hristov Stoychev Noëlani van den Berg Noëlani van den Berg Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism Frontiers in Microbiology SWATH-MS phosphite Phytophthora cinnamomi oxidoreductases metabolism antioxidants |
| title | Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| title_full | Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| title_fullStr | Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| title_full_unstemmed | Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| title_short | Phosphite inhibits Phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| title_sort | phosphite inhibits phytophthora cinnamomi by downregulating oxidoreductases and disrupting energy metabolism |
| topic | SWATH-MS phosphite Phytophthora cinnamomi oxidoreductases metabolism antioxidants |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1632726/full |
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