1. Leafhopper salivary carboxylesterase suppresses JA-Ile synthesis to facilitate initial arbovirus transmission in rice phloem.
- Author
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Chi Y, Zhang H, Chen S, Cheng Y, Zhang X, Jia D, Chen Q, Chen H, and Wei T
- Subjects
- Animals, Reoviridae physiology, Carboxylesterase metabolism, Carboxylesterase genetics, Plant Diseases virology, Insect Proteins metabolism, Insect Proteins genetics, Insect Vectors virology, Insect Vectors metabolism, Insect Vectors genetics, Plant Proteins metabolism, Plant Proteins genetics, Oxylipins metabolism, Oryza virology, Oryza genetics, Oryza metabolism, Hemiptera virology, Hemiptera genetics, Cyclopentanes metabolism, Phloem metabolism, Phloem virology, Isoleucine analogs & derivatives, Isoleucine metabolism
- Abstract
Plant jasmonoyl-L-isoleucine (JA-Ile) is a major defense signal against insect feeding, but whether or how insect salivary effectors suppress JA-Ile synthesis and thus facilitate viral transmission in the plant phloem remains elusive. Insect carboxylesterases (CarEs) are the third major family of detoxification enzymes. Here, we identify a new leafhopper CarE, CarE10, that is specifically expressed in salivary glands and is secreted into the rice phloem as a saliva component. Leafhopper CarE10 directly binds to rice jasmonate resistant 1 (JAR1) and promotes its degradation by the proteasome system. Moreover, the direct association of CarE10 with JAR1 clearly impairs JAR1 enzyme activity for conversion of JA to JA-Ile in an in vitro JA-Ile synthesis system. A devastating rice reovirus activates and promotes the co-secretion of virions and CarE10 via virus-induced vesicles into the saliva-storing salivary cavities of the leafhopper vector and ultimately into the rice phloem to establish initial infection. Furthermore, a virus-mediated increase in CarE10 secretion or overexpression of CarE10 in transgenic rice plants causes reduced levels of JAR1 and thus suppresses JA-Ile synthesis, promoting host attractiveness to insect vectors and facilitating initial viral transmission. Our findings provide insight into how the insect salivary protein CarE10 suppresses host JA-Ile synthesis to promote initial virus transmission in the rice phloem., (Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)
- Published
- 2024
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