Scavenging H2O2 of plant host by saliva catalase of leafhopper vector benefits viral transmission

Summary Catalase (CAT) is the main reactive oxygen species (ROS)‐scavenging enzyme in plants and insects. However, it remains elusive whether and how insect saliva CAT suppresses ROS‐mediated plant defense, thereby promoting initial virus transmission by insect vectors. Here, we investigated how lea...

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Vydané v:The New phytologist Ročník 243; číslo 6; s. 2368 - 2384
Hlavní autori: Zhang, Hongxiang, Chi, Yunhua, Chen, Siyu, Lv, Xinwei, Jia, Dongsheng, Chen, Qian, Wei, Taiyun
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: Lancaster Wiley Subscription Services, Inc 01.09.2024
Predmet:
Catalase
Disease transmission
Enzymatic activity
Enzyme activity
Expression vectors
Feeding
genetically modified organisms
Glands
H2O2
Host plants
Hydrogen peroxide
Insects
leafhopper
Phloem
Plant viruses
Plants
Reactive oxygen species
Recilia dorsalis
Reoviridae
Rice
Saliva
saliva proteins
Salivary gland
Salivary glands
Scavenging
secretion
Vectors
viral transmission
Virions
virus transmission
Viruses
ISSN:0028-646X, 1469-8137, 1469-8137
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Shrnutí:Summary Catalase (CAT) is the main reactive oxygen species (ROS)‐scavenging enzyme in plants and insects. However, it remains elusive whether and how insect saliva CAT suppresses ROS‐mediated plant defense, thereby promoting initial virus transmission by insect vectors. Here, we investigated how leafhopper Recilia dorsalis catalase (RdCAT) was secreted from insect salivary glands into rice phloem, and how it was perceived by rice chaperone NO CATALASE ACTIVITY1 (OsNCA1) to scavenge excessive H2O2 during insect‐to‐plant virus transmission. We found that the interaction of OsNCA1 with RdCAT activated its enzymatic activity to decompose H2O2 in rice plants during leafhopper feeding. However, initial insect feeding did not significantly change rice CATs transcripts. Knockout of OsNCA1 in transgenic lines decreased leafhopper feeding‐activated CAT activity and caused higher H2O2 accumulation. A devastating rice reovirus activated RdCAT expression and promoted the cosecretion of virions and RdCAT into leafhopper salivary cavities and ultimately into the phloem. Virus‐mediated increase of RdCAT secretion suppressed excessive H2O2, thereby promoting host attractiveness to insect vectors and initial virus transmission. Our findings provide insights into how insect saliva CAT is secreted and perceived by plant chaperones to suppress the early H2O2 burst during insect feeding, thereby facilitating viral transmission.
Bibliografia:These authors contributed equally to this work.
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ISSN:0028-646X
1469-8137
1469-8137
DOI:10.1111/nph.19988