Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs
Introduction: As an important herbivore-induced plant volatile, (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) is known for its defensive role against multiple insect pests, including attracting natural enemies. A terpene synthase (GhTPS14) and two cytochrome P450 (GhCYP82L1, GhCYP82L2) enzymes are invol...
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Elsevier
2025-05-01
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| Series: | Journal of Advanced Research |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2090123224002121 |
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| author | Dong Teng Danfeng Liu Adel Khashaveh Beibei Lv Peiyao Sun Ting Geng Hongzhi Cui Yi Wang Yongjun Zhang |
| author_facet | Dong Teng Danfeng Liu Adel Khashaveh Beibei Lv Peiyao Sun Ting Geng Hongzhi Cui Yi Wang Yongjun Zhang |
| author_sort | Dong Teng |
| collection | DOAJ |
| description | Introduction: As an important herbivore-induced plant volatile, (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) is known for its defensive role against multiple insect pests, including attracting natural enemies. A terpene synthase (GhTPS14) and two cytochrome P450 (GhCYP82L1, GhCYP82L2) enzymes are involved in the de novo synthesis of DMNT in cotton. We conducted a study to test the potential of manipulating DMNT-synthesizing enzymes to enhance plant resistance to insects. Objectives: To manipulate DMNT emissions in cotton and generate cotton lines with increased resistance to mirid bug Apolygus lucorum. Methods: Biosynthesis and emission of DMNT by cotton plants were altered using CRISPR/Cas9 and overexpression approaches. Dynamic headspace sampling and GC–MS analysis were used to collect, identify and quantify volatiles. The attractiveness and suitability of cotton lines against mirid bug and its parasitoid Peristenus spretus were evaluated through various assays. Results: No DMNT emission was detected in knockout CAS-L1L2 line, where both GhCYP82L1 and GhCYP82L2 were knocked out. In contrast, gene-overexpressed lines released higher amounts of DMNT when infested by A. lucorum. At the flowering stage, L114 (co-overexpressing GhCYP82L1 and GhTPS14) emitted 10–15-fold higher amounts than controls. DMNT emission in overexpressed transgenic lines could be triggered by methyl jasmonate (MeJA) treatment. Apolygus lucorum and its parasitoid were far less attracted to the double edited CAS-L1L2 plants, however, co-overexpressed line L114 significantly attracted bugs and female wasps. A high dose of DMNT, comparable to the emission of L114, significantly inhibited the growth of A. lucorum, and further resulted in higher mortalities. Conclusion: Turning down DMNT emission attenuated the behavioral preferences of A. lucorum to cotton. Genetically modified cotton plants with elevated DMNT emission not only recruited parasitoids to enhance indirect defense, but also formed an ecological trap to kill the bugs. Therefore, manipulation of DMNT biosynthesis and emission in plants presents a promising strategy for controlling mirid bugs. |
| format | Article |
| id | doaj-art-af4f4ab6d3bb4510a2c9e66aefe883db |
| institution | OA Journals |
| issn | 2090-1232 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Advanced Research |
| spelling | doaj-art-af4f4ab6d3bb4510a2c9e66aefe883db2025-08-20T02:19:51ZengElsevierJournal of Advanced Research2090-12322025-05-0171294110.1016/j.jare.2024.05.022Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugsDong Teng0Danfeng Liu1Adel Khashaveh2Beibei Lv3Peiyao Sun4Ting Geng5Hongzhi Cui6Yi Wang7Yongjun Zhang8State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaYunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming 650504, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China; Institute of Cotton Research, Shanxi Agricultural University, Yuncheng 044000, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaNational Plant Protection Scientific Observation and Experiment Station, Langfang 065000, ChinaBiocentury Transgene (China) Co. Ltd., Shenzhen 518117, ChinaYunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming 650504, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China; Corresponding author.Introduction: As an important herbivore-induced plant volatile, (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) is known for its defensive role against multiple insect pests, including attracting natural enemies. A terpene synthase (GhTPS14) and two cytochrome P450 (GhCYP82L1, GhCYP82L2) enzymes are involved in the de novo synthesis of DMNT in cotton. We conducted a study to test the potential of manipulating DMNT-synthesizing enzymes to enhance plant resistance to insects. Objectives: To manipulate DMNT emissions in cotton and generate cotton lines with increased resistance to mirid bug Apolygus lucorum. Methods: Biosynthesis and emission of DMNT by cotton plants were altered using CRISPR/Cas9 and overexpression approaches. Dynamic headspace sampling and GC–MS analysis were used to collect, identify and quantify volatiles. The attractiveness and suitability of cotton lines against mirid bug and its parasitoid Peristenus spretus were evaluated through various assays. Results: No DMNT emission was detected in knockout CAS-L1L2 line, where both GhCYP82L1 and GhCYP82L2 were knocked out. In contrast, gene-overexpressed lines released higher amounts of DMNT when infested by A. lucorum. At the flowering stage, L114 (co-overexpressing GhCYP82L1 and GhTPS14) emitted 10–15-fold higher amounts than controls. DMNT emission in overexpressed transgenic lines could be triggered by methyl jasmonate (MeJA) treatment. Apolygus lucorum and its parasitoid were far less attracted to the double edited CAS-L1L2 plants, however, co-overexpressed line L114 significantly attracted bugs and female wasps. A high dose of DMNT, comparable to the emission of L114, significantly inhibited the growth of A. lucorum, and further resulted in higher mortalities. Conclusion: Turning down DMNT emission attenuated the behavioral preferences of A. lucorum to cotton. Genetically modified cotton plants with elevated DMNT emission not only recruited parasitoids to enhance indirect defense, but also formed an ecological trap to kill the bugs. Therefore, manipulation of DMNT biosynthesis and emission in plants presents a promising strategy for controlling mirid bugs.http://www.sciencedirect.com/science/article/pii/S2090123224002121Plant defenseDMNT biosynthesisCRISPR/Cas9OverexpressionMirid bugEcological trap |
| spellingShingle | Dong Teng Danfeng Liu Adel Khashaveh Beibei Lv Peiyao Sun Ting Geng Hongzhi Cui Yi Wang Yongjun Zhang Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs Journal of Advanced Research Plant defense DMNT biosynthesis CRISPR/Cas9 Overexpression Mirid bug Ecological trap |
| title | Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs |
| title_full | Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs |
| title_fullStr | Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs |
| title_full_unstemmed | Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs |
| title_short | Engineering DMNT emission in cotton enhances direct and indirect defense against mirid bugs |
| title_sort | engineering dmnt emission in cotton enhances direct and indirect defense against mirid bugs |
| topic | Plant defense DMNT biosynthesis CRISPR/Cas9 Overexpression Mirid bug Ecological trap |
| url | http://www.sciencedirect.com/science/article/pii/S2090123224002121 |
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