A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

Abstract

ORCID IDs: 0000-0002-5714-7586 (J.Z.); 0000-0002-3262-6134 (Y.L.).The brown planthopper (BPH) Nilaparvata lugens is one of the most destructive insect pests on rice (Oryza sativa) in Asia. After landing on plants, BPH rapidly accesses plant phloem and sucks the phloem sap through unknown mechanisms. We discovered a salivary endo-b-1,4-glucanase (NlEG1) that has endoglucanase activity with a maximal activity at pH 6 at 37°C and is secreted into rice plants by BPH. NlEG1 is highly expressed in the salivary glands and midgut. Silencing NlEG1 decreases the capacity of BPH to reach the phloem and reduces its food intake, mass, survival, and fecundity on rice plants. By contrast, NlEG1 silencing had only a small effect on the survival rate of BPH raised on artificial diet. Moreover, NlEG1 secreted by BPH did not elicit the production of the defense-related signal molecules salicylic acid, jasmonic acid, and jasmonoyl-isoleucine in rice, although wounding plus the application of the recombination protein NlEG1 did slightly enhance the levels of jasmonic acid and jasmonoyl-isoleucine in plants compared with the corresponding controls. These data suggest that NlEG1 enables the BPH's stylet to reach the phloem by degrading celluloses in plant cell walls, thereby functioning as an effector that overcomes the plant cell wall defense in rice.

A Mucin-Like Protein of Planthopper Is Required for Feeding and Induces Immunity Response in Plants

“…Two secretary proteins that actively participate in salivary sheath formation were recently identified in BPHs (Huang et al, 2015. Furthermore, several salivary proteins that play important roles in interactions between BPH and rice were identified (Petrova and Smith, 2014;Ji et al, 2017;Ye et al, 2017). However, the functions of the majority of BPH-secreted proteins have not yet been experimentally determined.…”

Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defence

“…To investigate the effect of DNase II on the H 2 O 2 defence response of wounded plants, purified GFP and DNase II–GFP were applied to wounded rice plants as previously described (Ji et al ., ; Ye et al ., ). We found that the H 2 O 2 level in wounding plus GFP (14.6–15.4 nmol g −1 ) and wounding plus DNase II–GFP (14.3–17.6 nmol g −1 ) significantly increased when compared with the untreated control (8.2–10.6 nmol g −1 ) (Fig.…”

“…The bioactive components in herbivore saliva have been extensively investigated. For example, calcium‐binding proteins regulate the concentration of free ionic calcium (Will et al ., ); glucanases degrade celluloses in plant cell walls (Ji et al ., ); oxidoreductases detoxify secondary metabolic products and maintain ROS levels in plant tissues (Morgan et al ., ). Here, we reveal that the planthopper saliva can degrade DNA, and that the responsible enzyme is DNase II.…”

“…Untreated TN1 plants and plants that were pierced individually with a microcapillary 50 times on the lower part of the stems (wound treatment) were used as controls. Different substances (that is saliva collected from ds GFP or ds DNase II ‐treated SBPHs, recombinant proteins, mixture of saliva and recombinant proteins) were applied to the surface of the wounded plants as described previously (Ji et al ., ). For recombinant proteins, samples were diluted into 40 ng μl −1 , and 20 μl solution were applied.…”

Current understanding of the molecular players involved in resistance to rice planthoppers

“…Present data show that some BPH salivary proteins function as effectors. These include an endo‐ β ‐1,4‐glucanase, salivary DNase II and salivary EF‐hand calcium‐binding protein, which all inhibit the rice defense response to planthoppers. Conversely, some salivary proteins function as elicitors, such as the BPH‐secreted mucin‐like protein, which induces rice defense response against planthoppers.…”