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Sakuranetin protects rice from brown planthopper attack by depleting its beneficial endosymbionts

文献类型: 外文期刊

作者: Liu, Mengyu 1 ; Hong, Gaojie 2 ; Li, Huijing 1 ; Bing, Xiaoli 3 ; Chen, Yumeng 1 ; Jing, Xiangfeng 4 ; Gershenzon, Jonathan 5 ; Lou, Yonggen 1 ; Baldwin, Ian T. 6 ; Li, Ran 1 ;

作者机构: 1.Zhejiang Univ, Inst Insect Sci, State Key Lab Rice Biol, Key Lab Biol Crop Pathogens & Insects Zhejiang Pro, Hangzhou 310058, Peoples R China

2.Zhejiang Acad Agr Sci, Inst Virol & Biotechnol, Hangzhou 310021, Peoples R China

3.Nanjing Agr Univ, Coll Plant Protect, Dept Entomol, Nanjing 210095, Peoples R China

4.Northwest A&F Univ, Coll Plant Protect, State Key Lab Crop Stress Biol Arid Areas, Yangling 712100, Peoples R China

5.Max Planck Inst Chem Ecol, Dept Biochem, D-07745 Jena, Germany

6.Max Planck Inst Chem Ecol, Dept Mol Ecol, D-07745 Jena, Germany

关键词: rice; sakuranetin; beneficial endosymbionts; jasmonate signaling; direct defense

期刊名称:PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA ( 影响因子:11.1; 五年影响因子:12.0 )

ISSN: 0027-8424

年卷期: 2023 年 120 卷 23 期

页码:

收录情况: SCI

摘要: Plants produce chemical defenses that poison insect herbivores or deter their feeding, but herbivores are also accompanied by microbial endosymbionts crucial for their nutrition, reproduction, and fitness. Hence, plant defenses could target a herbivore's beneficial endosymbionts, but this has not yet been demonstrated. Here, we studied flavonoids that are induced when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH), which harbors beneficial yeast-like symbionts (YLS) essential for insect nutrition, such as by remedying deficiencies in sterols. BPH attack dramatically increased sakuranetin accumulations in leaf sheaths and phloem exudates. Sakuranetin is an antifungal phytoalexin derived from the antibacterial precursor, naringenin, via catalysis of naringenin-O-methyltransferase (NOMT). When added to artificial diets, sakuranetin decreased BPH survivorship, suggesting that it functions as an induced defense. Mutation of NOMT abolished sakuranetin accumulation and increased BPH oviposition and hatching rates. High-throughput amplicon sequencing revealed that BPH fed on sakuranetin-deficient nomt lines were enriched in YLS with only minor changes in the bacterial endosymbionts, compared to those feeding on sakuranetin-rich wild-type (WT) plants. In-vitro feeding of sakuranetin suggested that this flavonoid directly inhibited the growth of YLS. BPH feeding on nomt lines accumulated higher cholesterol levels, which might be attributed to increases in the supply of sterol precursors from the YLS, while nomt lines suffered more damage than WT plants did from BPH herbivory. BPH-elicited accumulation of sakuranetin requires intact jasmonate (JA) signaling. This study reveals that rice uses a JA-induced antifungal flavonoid phytoalexin in defense against BPH by inhibiting its beneficial endosymbionts.

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