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Proc Natl Acad Sci U S A


Title:Sakuranetin protects rice from brown planthopper attack by depleting its beneficial endosymbionts
Author(s):Liu M; Hong G; Li H; Bing X; Chen Y; Jing X; Gershenzon J; Lou Y; Baldwin IT; Li R;
Address:"State Key Laboratory of Rice Biology, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China. Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China. Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China. State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling 712100, China. Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena 07745, Germany. Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena 07745, Germany"
Journal Title:Proc Natl Acad Sci U S A
Year:2023
Volume:20230531
Issue:23
Page Number:e2305007120 -
DOI: 10.1073/pnas.2305007120
ISSN/ISBN:1091-6490 (Electronic) 0027-8424 (Print) 0027-8424 (Linking)
Abstract:"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"
Keywords:"Animals Female Antifungal Agents Flavonoids/pharmacology Gene Expression Regulation, Plant *Hemiptera *Oryza/genetics beneficial endosymbionts direct defense jasmonate signaling rice sakuranetin;"
Notes:"MedlineLiu, Mengyu Hong, Gaojie Li, Huijing Bing, Xiaoli Chen, Yumeng Jing, Xiangfeng Gershenzon, Jonathan Lou, Yonggen Baldwin, Ian T Li, Ran eng Research Support, Non-U.S. Gov't 2023/05/31 Proc Natl Acad Sci U S A. 2023 Jun 6; 120(23):e2305007120. doi: 10.1073/pnas.2305007120. Epub 2023 May 31"

 
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