A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice

Abstract

nature biotechnology advance online publication l e t t e r sThe brown planthopper (BPH) is the most destructive pest of rice (Oryza sativa) and a substantial threat to rice production, causing losses of billions of dollars annually 1,2 . Breeding of resistant cultivars is currently hampered by the rapid breakdown of BPH resistance 2 . Thus, there is an urgent need to identify more effective BPH-resistance genes. Here, we report molecular cloning and characterization of Bph3, a locus in rice identified more than 30 years ago that confers resistance to BPH. We show that Bph3 is a cluster of three genes encoding plasma membrane-localized lectin receptor kinases (OsLecRK1-OsLecRK3). Introgression of Bph3 into susceptible rice varieties by transgenic or marker-assisted selection strategies significantly enhanced resistance to both the BPH and the white back planthopper. Our results suggest that these lectin receptor kinase genes function together to confer broad-spectrum and durable insect resistance and provide a resource for molecular breeding of insect-resistant rice cultivars.BPH (Nilaparvata lugens Stål, Hemiptera, Delphacidae) is a monophagous, phloem-sucking herbivore. It sucks the sap from the rice phloem using its stylet, and causes direct damage to rice plants. BPH can also cause indirect damage to rice plants through the transmission of viruses including the rice ragged stunt virus and grassy stunt virus 2 . Repeated overapplication of pesticides for BPH management has heavily polluted the environment 3 . Breeding of resistant cultivars is the most cost-effective and environmentally responsible strategy for BPH management but developing insect resistant cultivars by traditional breeding approaches is extremely difficult and time consuming owing to a paucity of knowledge about BPH resistance genes and germplasm.To date, 28 BPH resistance loci have been identified from cultivated and wild species of Oryza 2,4,5 . Only two of these resistance genes, Bph14 and Bph26 have been cloned to date 6,7 . In addition, BPH resistance of IR26 and IR36, two widely cultivated rice varieties that harbor the BPH resistance loci Bph1 and bph2, respectively, was quickly broken down in just a few years owing to the rapid adaptation of the BPH 8 . Thus, there is still an urgent need to identify new types of resistance genes and germplasm for developing efficient approaches to breed broad-spectrum and durable BPH-resistant rice cultivars. Notably, the Bph3 locus, originally identified in the Sri Lankan indica cultivar Rathu Heenati 9 , displayed resistance to four BPH biotypes (BPH biotypes refer to specific populations of BPH classified according to their virulence on different BPH resistance genes) 2,10 . Furthermore, rice varieties harboring Bph3 deployed more than 30 years ago in the Philippines are still resistant to BPH 8 . However, the molecular basis of this broad-spectrum and durable resistance of Bph3 against BPH remains unknown.We observed that Bph3-containing Rathu Heenati infested with BPH of mixed biotypes (biotype ...

Allelic diversity in an NLR geneBPH9enables rice to combat planthopper variation

“…In this study, we showed that insect-resistance genes clustered on chromosome 12L are actually multialleles. For those BPH-resistance genes on chromosome 4S, at least two, BPH3 and BPH15, have been identified to encode lectin receptor kinases (13,39). Rice appears to adapt the same strategy in the coevolution war to insect pests as to pathogens.…”

“…Interestingly, most of these genes are mapped on several chromosome regions in clusters (12)(13)(14). The cluster on the long arm of chromosome 12 (12L) is the largest one that harbors eight BPHresistance genes, including the most widely used BPH1 and BPH2 (12,14).…”

Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C4grass

“…5B)-DREBs are the most extensively studied drought-responsive group of genes in Arabidopsis (Sakuma et al 2002;Agarwal et al 2006;Xianjun et al 2011); (3) FT, a central gene in the flowering pathway (Fig. 5C)-several recent studies have implicated a physiological and genetic tie between drought-responsive and flowering pathways (McKay et al 2003;Lovell et al 2013Lovell et al , 2015Riboni et al 2013;Kimura et al 2015); (4) RLK1, the rice ortholog (OsLecRK4) which improves resistance to insect herbivory (Liu et al 2015), and (5) a rice ortholog (OSMate2) of the MATE efflux family gene AT1G71140, which, when overexpressed in A. thaliana, alters a variety of abiotic and biotic stress responses (Tiwari et al 2014). …”

Pattern Recognition Receptors—Versatile Genetic Tools for Engineering Broad-Spectrum Disease Resistance in Crops

“…Furthermore, the identification of various PRRs for chemically diverse types of MAMPs has revealed that plant PRRs are typically RLKs or RLPs. Thus, these protein families can now also be systematically tested for a putative role in plant immunity, for instance through screening for altered resistance against the pathogen of interest in loss-or gain-of-function mutants or natural accessions, or through heterologous expression in suitable model plants (e.g., Arabidopsis thaliana or N. benthamiana) [64][65][66][67][68][69].…”