A tripartite rheostat controls self-regulated host plant resistance to insects

Abstract

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 Stål) 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.

Rapid intracellular acidification is a novel plant defense response countered by the brown planthopper

“…Pathogen/insect-derived effectors can be powerful molecular probes to discovering novel plant regulators/responses to biotic attacks. Although other piercing/sucking herbivores derived effectors, such as Btfer1, LsPDI1, LsSP1, Mp55, DNase II and BISP, have been reported as defense-suppressive effectors, 33-38 our discovery of intracellular acidification as a plant defense response and our finding that brown planthopper (BPH) secretes NICA as a counter-defense measure illustrates host cell pH homeostasis as a novel battlefield that has not been revealed in any plant-biotic interactions.…”

Recent Advances in Molecular Mechanism and Breeding Utilization of Brown Planthopper Resistance Genes in Rice: An Integrated Review

“…Further research has revealed that the carboxyl terminal of NlMLP regulates Ca 2+ flux and the JA signaling pathway, activating the expression of defense-related genes and inducing callose deposition [95]. Guo et al (2023) identified and characterized the first insect salivary protein perceived by the plant immune receptor, which is a saliva protein BISP (BPH14interacting salivary protein) of the brown planthopper (BPH) [96]. In susceptible varieties, [92], and complementing and perfecting the molecular network mechanism related to all BPH-resistant genes].…”

“…In susceptible varieties, BISP targets OsRLCK185 and inhibits the basic defense. In varieties carrying the brown planthopper resistance gene Bph14, Bph14 binds to BISP and activates the host immune response but inhibits rice growth [96]. BISP-Bph14 binds to the selective autophagic cargo receptor OsNBR1 and results in the degradation of BISP through the autophagic pathway, downregulating rice resistance against BPH and restoring the plant growth [96].…”

“…In varieties carrying the brown planthopper resistance gene Bph14, Bph14 binds to BISP and activates the host immune response but inhibits rice growth [96]. BISP-Bph14 binds to the selective autophagic cargo receptor OsNBR1 and results in the degradation of BISP through the autophagic pathway, downregulating rice resistance against BPH and restoring the plant growth [96]. This study reveals the molecular mechanism underlying the balance of immunity and growth in the BISP-BPH14-OsNBR1 interaction system by perceiving and regulating the protein level of insect effectors.…”

A mechanism for fine-tuning host rice resistance based on the feeding behavior of brown planthoppe

“…BPH14互作. 该蛋白命名为BPH14-Interacting Salivary Protein (BISP) [9] . BISP在褐飞虱唾液腺中高表达, 在褐飞虱取食时被 图 1 (网络版彩色)BISP诱导的免疫调节模型 [9] .…”