A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice

Wenfeng Ye,Haixin Yu,Rui Ji,Jiamei Zeng,Yukun Jian,Hongdan Chen,Yonggen Lou

doi:10.1038/srep40498

Wenfeng Ye, Haixin Yu + Show 5 more

Open Access

https://doi.org/10.1038/srep40498

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Abstract

The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), a major pest of rice in Asia, is able to successfully puncture sieve tubes in rice with its piercing stylet and then to ingest phloem sap. How BPH manages to continuously feed on rice remains unclear. Here, we cloned the gene NlSEF1, which is highly expressed in the salivary glands of BPH. The NlSEF1 protein has EF-hand Ca2+-binding activity and can be secreted into rice plants when BPH feed. Infestation of rice by BPH nymphs whose NlSEF1 was knocked down elicited higher levels of Ca2+ and H2O2 but not jasmonic acid, jasmonoyl-isoleucine (JA-Ile) and SA in rice than did infestation by control nymphs; Consistently, wounding plus the recombination protein NlSEF1 suppressed the production of H2O2 in rice. Bioassays revealed that NlSEF1-knockdown BPH nymphs had a higher mortality rate and lower feeding capacity on rice than control nymphs. These results indicate that the salivary protein in BPH, NlSEF1, functions as an effector and plays important roles in interactions between BPH and rice by mediating the plant’s defense responses.

Highlights

In nature, plants are constantly threatened by herbivorous insects
Based on the data from transcriptomes of brown planthopper (BPH) salivary glands[23], the open reading frame (ORF) (726 bp) of the gene NlSEF1 was obtained by reverse-transcription-polymerase chain reaction (RT-PCR) (Fig. 1, GenBank: KT698079)
NlSEF1, containing two EF-hand motifs in its C-terminus, can be injected into rice plants when BPH are feeding (Fig. 4B). This result implies that NlSEF1 may play an important role in rice-BPH interactions

Summary

Introduction

Plants are constantly threatened by herbivorous insects. plants have evolved both constitutive and induced defenses that appear after herbivore attack[1]. Inducible defenses begin with the recognition of specific herbivore-associated molecular patterns (HAMPs) and are followed by the elicitation of a complex signaling network, consisting mainly of mitogen-activated protein kinase (MAPK) cascades, and jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) signaling pathways, which subsequently results in the reconfiguration of the transcriptome and proteasome as well as the biosynthesis of defensive chemicals[2,3]. This HAMP-triggered immunity (HTI) is effective with some herbivore populations but not with herbivores that secrete effectors which can effectively suppress the HTI3. Whether these putative salivary proteins influence plant defense and mediate the feeding ability of BPH remains unclear

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