Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut
Aflatoxins are immunosuppressive and carcinogenic secondary metabolites, produced by the filamentous ascomycete <i>Aspergillus flavus</i>, that are hazardous to animal and human health. In this study, we show that multiplexed host-induced gene silencing (HIGS) of <i>Aspergillus fla...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-05-01
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| Series: | Toxins |
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| Online Access: | https://www.mdpi.com/2072-6651/15/5/319 |
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| author | Kalyani Prasad Kalenahalli Yogendra Hemalatha Sanivarapu Kanniah Rajasekaran Jeffrey W. Cary Kiran K. Sharma Pooja Bhatnagar-Mathur |
| author_facet | Kalyani Prasad Kalenahalli Yogendra Hemalatha Sanivarapu Kanniah Rajasekaran Jeffrey W. Cary Kiran K. Sharma Pooja Bhatnagar-Mathur |
| author_sort | Kalyani Prasad |
| collection | DOAJ |
| description | Aflatoxins are immunosuppressive and carcinogenic secondary metabolites, produced by the filamentous ascomycete <i>Aspergillus flavus</i>, that are hazardous to animal and human health. In this study, we show that multiplexed host-induced gene silencing (HIGS) of <i>Aspergillus flavus</i> genes essential for fungal sporulation and aflatoxin production (<i>nsdC</i>, <i>veA</i>, <i>aflR</i>, and <i>aflM)</i> confers enhanced resistance to <i>Aspergillus</i> infection and aflatoxin contamination in groundnut (<20 ppb). Comparative proteomic analysis of contrasting groundnut genotypes (WT and near-isogenic HIGS lines) supported a better understanding of the molecular processes underlying the induced resistance and identified several groundnut metabolites that might play a significant role in resistance to <i>Aspergillus</i> infection and aflatoxin contamination. Fungal differentiation and pathogenicity proteins, including calmodulin, transcriptional activator-HacA, kynurenine 3-monooxygenase 2, VeA, VelC, and several aflatoxin pathway biosynthetic enzymes, were downregulated in <i>Aspergillus</i> infecting the HIGS lines. Additionally, in the resistant HIGS lines, a number of host resistance proteins associated with fatty acid metabolism were strongly induced, including phosphatidylinositol phosphate kinase, lysophosphatidic acyltransferase-5, palmitoyl-monogalactosyldiacylglycerol Δ-7 desaturase, ceramide kinase-related protein, sphingolipid Δ-8 desaturase, and phospholipase-D. Combined, this knowledge can be used for groundnut pre-breeding and breeding programs to provide a safe and secure food supply. |
| first_indexed | 2024-03-11T03:15:22Z |
| format | Article |
| id | doaj.art-581cfa6833b64f0b9225c9c125e4a166 |
| institution | Directory Open Access Journal |
| issn | 2072-6651 |
| language | English |
| last_indexed | 2024-03-11T03:15:22Z |
| publishDate | 2023-05-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Toxins |
| spelling | doaj.art-581cfa6833b64f0b9225c9c125e4a1662023-11-18T03:33:21ZengMDPI AGToxins2072-66512023-05-0115531910.3390/toxins15050319Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in GroundnutKalyani Prasad0Kalenahalli Yogendra1Hemalatha Sanivarapu2Kanniah Rajasekaran3Jeffrey W. Cary4Kiran K. Sharma5Pooja Bhatnagar-Mathur6International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad 502324, IndiaInternational Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad 502324, IndiaInternational Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad 502324, IndiaSouthern Regional Research Center, Agricultural Research Service, United States Department of Agriculture (USDA/ARS), New Orleans, LA 70124, USASouthern Regional Research Center, Agricultural Research Service, United States Department of Agriculture (USDA/ARS), New Orleans, LA 70124, USASustainable Agriculture Program, The Energy and Resources Institute (TERI), India Habitat Center, New Delhi 110003, IndiaInternational Maize and Wheat Improvement Center (CIMMYT), El Batán, Texcoco 56237, MexicoAflatoxins are immunosuppressive and carcinogenic secondary metabolites, produced by the filamentous ascomycete <i>Aspergillus flavus</i>, that are hazardous to animal and human health. In this study, we show that multiplexed host-induced gene silencing (HIGS) of <i>Aspergillus flavus</i> genes essential for fungal sporulation and aflatoxin production (<i>nsdC</i>, <i>veA</i>, <i>aflR</i>, and <i>aflM)</i> confers enhanced resistance to <i>Aspergillus</i> infection and aflatoxin contamination in groundnut (<20 ppb). Comparative proteomic analysis of contrasting groundnut genotypes (WT and near-isogenic HIGS lines) supported a better understanding of the molecular processes underlying the induced resistance and identified several groundnut metabolites that might play a significant role in resistance to <i>Aspergillus</i> infection and aflatoxin contamination. Fungal differentiation and pathogenicity proteins, including calmodulin, transcriptional activator-HacA, kynurenine 3-monooxygenase 2, VeA, VelC, and several aflatoxin pathway biosynthetic enzymes, were downregulated in <i>Aspergillus</i> infecting the HIGS lines. Additionally, in the resistant HIGS lines, a number of host resistance proteins associated with fatty acid metabolism were strongly induced, including phosphatidylinositol phosphate kinase, lysophosphatidic acyltransferase-5, palmitoyl-monogalactosyldiacylglycerol Δ-7 desaturase, ceramide kinase-related protein, sphingolipid Δ-8 desaturase, and phospholipase-D. Combined, this knowledge can be used for groundnut pre-breeding and breeding programs to provide a safe and secure food supply.https://www.mdpi.com/2072-6651/15/5/319aflatoxin<i>Arachis hypogaea</i> L.<i>Aspergillus flavus</i>fatty acidhost-induced gene silencinggroundnut |
| spellingShingle | Kalyani Prasad Kalenahalli Yogendra Hemalatha Sanivarapu Kanniah Rajasekaran Jeffrey W. Cary Kiran K. Sharma Pooja Bhatnagar-Mathur Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut Toxins aflatoxin <i>Arachis hypogaea</i> L. <i>Aspergillus flavus</i> fatty acid host-induced gene silencing groundnut |
| title | Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut |
| title_full | Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut |
| title_fullStr | Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut |
| title_full_unstemmed | Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut |
| title_short | Multiplexed Host-Induced Gene Silencing of <i>Aspergillus flavus</i> Genes Confers Aflatoxin Resistance in Groundnut |
| title_sort | multiplexed host induced gene silencing of i aspergillus flavus i genes confers aflatoxin resistance in groundnut |
| topic | aflatoxin <i>Arachis hypogaea</i> L. <i>Aspergillus flavus</i> fatty acid host-induced gene silencing groundnut |
| url | https://www.mdpi.com/2072-6651/15/5/319 |
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