Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice

Abstract

The brown planthopper (BPH) and white-backed planthopper (WBPH) are the most destructive insect pests of rice, and they pose serious threats to rice production throughout Asia. Thus, there are urgent needs to identify resistance-conferring genes and to breed planthopper-resistant rice varieties. Here we report the map-based cloning and functional analysis of Bph6, a gene that confers resistance to planthoppers in rice. Bph6 encodes a previously uncharacterized protein that localizes to exocysts and interacts with the exocyst subunit OsEXO70E1. Bph6 expression increases exocytosis and participates in cell wall maintenance and reinforcement. A coordinated cytokinin, salicylic acid and jasmonic acid signaling pathway is activated in Bph6-carrying plants, which display broad resistance to all tested BPH biotypes and to WBPH without sacrificing yield, as these plants were found to maintain a high level of performance in a field that was heavily infested with BPH. Our results suggest that a superior resistance gene that evolved long ago in a region where planthoppers are found year round could be very valuable for controlling agricultural insect pests.

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

“…Moreover, three unnamed recessive genes for BPH resistance have been reported from two newly identified rice germplasm sources (PHS29 and MRST3) . Furthermore, four BPH resistance genes in rice have been newly cloned by a map‐based cloning strategy over the latest years, including Bph6 , Bph9 , Bph18 and Bph32 . Among the eight cloned BPH resistance genes in rice, Bph3 , Bph6 , Bph9 , Bph14 , Bph18 , Bph26 , Bph29 and Bph32 , only Bph29 is a recessive resistance gene .…”

“…Furthermore, four BPH resistance genes in rice have been newly cloned by a map‐based cloning strategy over the latest years, including Bph6 , Bph9 , Bph18 and Bph32 . Among the eight cloned BPH resistance genes in rice, Bph3 , Bph6 , Bph9 , Bph14 , Bph18 , Bph26 , Bph29 and Bph32 , only Bph29 is a recessive resistance gene . Both Bph3 and Bph6 confer broad resistance to BPH and WBPH, whereas the remaining six genes confer resistance to BPH only .…”

“…Antixenosis, antibiosis and tolerance are three mechanistic types of host‐plant resistance to insects . Bph6 , Bph9 and Bph18 confer both antixenosis and antibiosis to BPH, whereas the remaining five genes confer BPH antibiosis only …”

“…WRKY46 and WRKY72 then bind to the promoters of defense genes (the receptor‐like cytoplasmic kinase gene RLCK281 and callose synthase gene LOC_Os01g67364.1) and potentiate the expression of these defense genes, resulting in enhanced resistance of rice to BPH . Bph6 encodes an exocyst‐localized protein and interacts with the OsEXO70E1 subunit of the exocyst, regulating the exocytosis of cells and maintaining the integrity of cell wall, thereby preventing the BPH and WBPH from sucking the sap from rice phloem, thus providing rice resistance to BPH and WBPH . The elucidation of action mechanisms of Bph6 first expands that the plant cell wall mediates the defense against planthopper and that exocyst complex acts as an important battleground in rice–planthopper interaction .…”

“…As evidenced by the five cloned planthopper resistance genes in rice, Bph6 , Bph9 , Bph14 , Bph26 and Bph29 , rice can respond effectively to planthopper infestation by activating a defense‐related signaling network, for example the salicylate signaling pathway was activated in rice when exposed to BPH (Table ). During the activation of signaling networks and expression of defense‐related genes, transcription factors play an important role, for example the transcription factors WRKY46 and WRKY72 potentiate defense gene expressions and rice immune responses .…”