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Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses

Rui Ji, Jianmei Fu, Yu Shi, Jìng Li, Maofeng Jing, Lu Wang, Shiying Yang, Tian Tian, Lihua Wang, Jia‐Fei Ju, Huifang Guo, Bin Liu, Daolong Dou, Ary A. Hoffmann, Keyan Zhu‐Salzman, Jichao Fang

2021New Phytologist98 citationsDOIOpen Access PDF

Abstract

Summary Vitellogenin (Vg) is a well‐known nutritious protein involved in reproduction in nearly all oviparous animals, including insects. Recently, Vg has been detected in saliva proteomes of several piercing–sucking herbivorous arthropods, including the small brown planthopper ( Laodelphax striatellus , SBPH). Its function, however, remains unexplored. We investigated the molecular mechanism underlying SBPH orally secreted Vg‐mediated manipulation of plant–insect interaction by RNA interference, phytohormone and H 2 O 2 profiling, protein–protein interaction studies and herbivore bioassays. A C‐terminal polypeptide of Vg (VgC) in SBPH, when secreted into rice plants, acted as a novel effector to attenuate host rice defenses, which in turn improved insect feeding performance. Silencing Vg reduced insect feeding and survival on rice. Vg ‐silenced SBPH nymphs consistently elicited higher H 2 O 2 production, a well‐established defense mechanism in rice, whereas expression of VgC in planta significantly hindered hydrogen peroxide (H 2 O 2 ) accumulation and promoted insect performance. VgC interacted directly with the rice transcription factor OsWRKY71, a protein which is involved in induction of H 2 O 2 accumulation and plant resistance to SBPH. These findings indicate a novel effector function of Vg: when secreted into host rice plants, this protein effectively weakened H 2 O 2 ‐mediated plant defense through its association with a plant immunity regulator.

Topics & Concepts

Brown planthopperBiologyEffectorVitellogeninNicotiana benthamianaInsectPlant defense against herbivoryCell biologyRNA interferenceOryza sativaBioassayOryzaBotanyBiochemistryRNAGeneEcologyInsect-Plant Interactions and ControlPlant Parasitism and ResistanceInsect symbiosis and bacterial influences
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