Abstract

The brown planthopper (BPH), Nilaparvata lugens Stål, is one of the major pests of rice. It uses its stylet to penetrate rice phloem, feeding on rice sap and causing direct damage to rice or even plant death. During the feeding process, BPHs secrete saliva into plant tissues, which plays crucial roles in the plant-insect interactions. However, little is known about how the salivary proteins secreted by BPH affect feeding ability and how they induce plant immune responses. Here, we identified an N. lugens Salivary Protein 1 (NlSP1) by screening salivary proteome and characterized its functions in BPH and plants. NlSP1 induces cell death, H2O2 accumulation, the expression of defense-related genes, and callose deposition in planta. The active region of NlSP1 that induces plant cell death is located in its N-terminal region. Inhibition of NlSP1 expression in BPHs reduced their feeding ability and had a lethal effect on them. Most importantly, we demonstrated that NlSP1 was able to be secreted into rice plant during feeding process and form a complex with certain interacting partner of rice. These results provide a detailed characterization of a salivary protein from BPHs and offers new insights into our understanding of rice-BPH interaction.

Highlights

  • The war between plants and herbivorous insects has a long history and continues

  • brown planthopper (BPH) repeatedly secrete both gelling and watery saliva from their salivary glands into plant cells, which plays a crucial role in plant-insect interactions

  • To further comprehensively explore candidate effector proteins of N. lugens, we combined salivary proteome identified in this study (Supplemental Table S1) with previously reported datum—BPH salivary proteome (Huang et al, 2016) and watery salivary proteome (Liu et al, 2016), and excluded those have been studied by secretome analysis (Rao et al, 2019)

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Summary

Introduction

The war between plants and herbivorous insects has a long history and continues. Herbivorous insects prey on plants by chewing or piercing-sucking and plants defense against herbivorous insects (Ehrlich and Raven, 1964). To protect themselves from injury by herbivores, plants have evolved sophisticated systems for resistance to herbivorous insects, including constitutive and induced defenses (Felton and Tumlinson, 2008; Erb et al, 2012; Mithöefer and Boland, 2012; Stam et al, 2014; Schuman and Baldwin, 2016). Constitutive defenses are the physical and chemical defense characteristic of plants without the influence of herbivorous insects. Induced defenses are installed only after the plant attacked by herbivores (Wu and Baldwin, 2010).

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