Plants deploy receptor-like kinases and nucleotide-binding leucine-rich repeat receptors to confer host plant resistance (HPR) to herbivores1. These gene-for-gene interactions between insects and their hosts have been proposed for more than 50 years2. However, the molecular and cellular mechanisms that underlie HPR have been elusive, as the identity and sensing mechanisms of insect avirulence effectors have remained unknown. Here we identify an insect salivary protein perceived by a plant immune receptor. The BPH14-interacting salivary protein (BISP) from the brown planthopper (Nilaparvata lugens St?l) is secreted into rice (Oryza sativa) during feeding. In susceptible plants, BISP targets O. satvia RLCK185 (OsRLCK185; hereafter Os is used to denote O. satvia-related proteins or genes) to suppress basal defences. In resistant plants, the nucleotide-binding leucine-rich repeat receptor BPH14 directly binds BISP to activate HPR. Constitutive activation of Bph14-mediated immunity is detrimental to plant growth and productivity. The fine-tuning of Bph14-mediated HPR is achieved through direct binding of BISP and BPH14 to the selective autophagy cargo receptor OsNBR1, which delivers BISP to OsATG8 for degradation. Autophagy therefore controls BISP levels. In Bph14 plants, autophagy restores cellular homeostasis by downregulating HPR when feeding by brown planthoppers ceases. We identify an insect saliva protein sensed by a plant immune receptor and discover a three-way interaction system that offers opportunities for developing high-yield, insect-resistant crops.
在植物與昆蟲的長期軍備競賽中，植物已經(jīng)發(fā)展出復雜的防御系統(tǒng)來對抗植食性昆蟲危害。植物利用類受體蛋白激酶（receptor-like kinases）和細胞內(nèi)NLR（nucleotide-binding leucine-rich repeat）受體賦予寄主植物對植食性害蟲的抗性(host-plant resistance, HPR）。植食性昆蟲取食過程中，向寄主植物分泌唾液以促進自身的取食。過去的十幾年間，植物體內(nèi)直接或間接監(jiān)測昆蟲效應蛋白（effector）的NLR受體已被成功分離，然而，被植物NLR識別并觸發(fā)寄主抗蟲反應的昆蟲效應蛋白一直未被發(fā)現(xiàn)。寄主植物如何識別昆蟲，并精密部署和調(diào)節(jié)自身抗性的機制仍未可知。該研究發(fā)現(xiàn)了首個被植物抗蟲蛋白識別并激活抗性反應的昆蟲效應子，并揭示了BISP-BPH14-OsNBR1互作系統(tǒng)精細調(diào)控抗性-生長平衡的新機制，為開發(fā)高產(chǎn)、抗蟲水稻品種提供了重大理論和應用基礎，也為其它糧食作物新型抗蟲、抗病機理的研究提供了新思路。
褐飛虱是水稻生產(chǎn)中的首要害蟲，常年肆虐我國及世界各國稻區(qū)，直接吸食水稻汁液并傳播病毒病，引起植株枯萎死亡，嚴重時導致顆粒無收。利用寄主植物抗性控制褐飛虱的侵害是重要措施。何光存教授課題組應用圖位克隆法在國際上首次分離了水稻抗褐飛虱基因Bph14。該基因編碼一個NLR蛋白。該研究通過酵母雙雜交篩選到與BPH14互作的褐飛虱唾液蛋白BISP（BPH14-Interacting Salivary Protein）。BISP在褐飛虱唾液腺中大量表達，并隨褐飛虱的取食被分泌到水稻組織。
該研究發(fā)現(xiàn)，BISP被褐飛虱分泌進入水稻后與水稻細胞質(zhì)激酶OsRLCK185結(jié)合，降低OsRLCK185的激酶活性從而抑制水稻基礎防御反應。另外，褐飛虱取食含Bph14的水稻過程中，BISP作為昆蟲效應子被BPH14識別并激活抗蟲反應。植物抗性的持續(xù)激活往往為生長發(fā)育帶來不利影響，因此，水稻需要精細調(diào)控自身抗蟲反應以兼顧自身的正常生長發(fā)育。
該研究結(jié)果表明，BISP進入水稻與BPH14互作，并與細胞自噬受體OsNBR1結(jié)合，OsNBR1與OsATG8的進一步結(jié)合，最終導致BISP經(jīng)自噬途徑降解。當褐飛虱停止取食后，水稻組織中殘留的BISP蛋白在48h內(nèi)被完全降解，使Bph14介導的抗蟲反應強度下降直至終止，恢復水稻的正常生長發(fā)育。BISP-BPH14-OsNBR1互作系統(tǒng)精細調(diào)控抗性-生長平衡的新機制，既促進了水稻的抗蟲功能又能不影響水稻產(chǎn)量。