Genome-Wide Mapping of Virulence in Brown Planthopper Identifies Loci That Break Down Host Plant Resistance

Abstract

Insects and plants have coexisted for over 350 million years and their interactions have affected ecosystems and agricultural practices worldwide. Variation in herbivorous insects' virulence to circumvent host resistance has been extensively documented. However, despite decades of investigation, the genetic foundations of virulence are currently unknown. The brown planthopper (Nilaparvata lugens) is the most destructive rice (Oryza sativa) pest in the world. The identification of the resistance gene Bph1 and its introduction in commercial rice varieties prompted the emergence of a new virulent brown planthopper biotype that was able to break the resistance conferred by Bph1. In this study, we aimed to construct a high density linkage map for the brown planthopper and identify the loci responsible for its virulence in order to determine their genetic architecture. Based on genotyping data for hundreds of molecular markers in three mapping populations, we constructed the most comprehensive linkage map available for this species, covering 96.6% of its genome. Fifteen chromosomes were anchored with 124 gene-specific markers. Using genome-wide scanning and interval mapping, the Qhp7 locus that governs preference for Bph1 plants was mapped to a 0.1 cM region of chromosome 7. In addition, two major QTLs that govern the rate of insect growth on resistant rice plants were identified on chromosomes 5 (Qgr5) and 14 (Qgr14). This is the first study to successfully locate virulence in the genome of this important agricultural insect by marker-based genetic mapping. Our results show that the virulence which overcomes the resistance conferred by Bph1 is controlled by a few major genes and that the components of virulence originate from independent genetic characters. The isolation of these loci will enable the elucidation of the molecular mechanisms underpinning the rice-brown planthopper interaction and facilitate the development of durable approaches for controlling this most destructive agricultural insect.

Chromosomal Location of a Recessive Red-Eye Mutant Gene in the Brown Planthopper <i>Nilaparvata lugens</i> (Stål) (Insecta: Hemiptera)

“…A genetic linkage map was constructed based on the segregation data. Finally, the red gene was mapped to a location between SSR markers BM20 and NLGS182 (Figure 4) on chromosome 9 according to Jing et al's map [10] or to the linkage group 2 according to our previous map [9]. This is the first study to successfully locate the red gene in the genome of this important insect pest of rice using markerbased genetic mapping.…”

“…Based on the presence of eye color of the BPH, we generated two groups of 29 brown-eyed (B) and 29 red-eyed (R) progenies from the F 2 population. A total of 387 SSR markers from Jairin et al [9] and Jing et al [10] covering 14 chromosomes of the BPH were selected to identify the R and B groups. The genetic linkage map was calculated by Join Map 4 [15] using genotype data from 95 F 2 individuals derived from crosses of KLS13/KBI13.…”

“…We employed an additional 20 SSR markers surrounding the BM20 locus on chromosome 9 [10] to assay 95 F 2 offspring. To obtain accurate estimates of marker positions on the map, we only selected clearly polymorphic markers and carefully scored them to reduce errors.…”

“…Numerous DNA markers were developed [9] [10] that made it possible to identify and map some genes in the BPH through linkage to existing DNA markers [10] [11]. In the present study, bulked segregant analysis (BSA) [12] with SSR markers was used to detect and locate the chromosomal location of the red gene controlling the red eye mutation in the BPH.…”

Geographic and Research Center Origins of Rice Resistance to Asian Planthoppers and Leafhoppers: Implications for Rice Breeding and Gene Deployment

“…Similarly, combining genes introgressed from wild rice species together with those from traditional varieties might improve durability; however, resistance genes from wild rice have been shown to be ineffective against certain planthopper populations, despite never having been deployed in farmers' fields. These recommendations assume that virulence to major genes is determined by gene-for-gene mechanisms [48,49]. However, if planthoppers adapt to defense mechanisms (irrespective of underlying genetics) then pyramiding arbitrary gene combinations might play little role in determining durability.…”