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

Abstract

This study examines aspects of virulence to resistant rice varieties among planthoppers and leafhoppers. Using a series of resistant varieties, brown planthopper, Nilaparvata lugens, virulence was assessed in seedlings and early-tillering plants at seven research centers in South and East Asia. Virulence of the whitebacked planthopper, Sogatella furcifera, in Taiwan and the Philippines was also assessed. Phylogenetic analysis of the varieties using single-nucleotide polymorphisms (SNPs) indicated a clade of highly resistant varieties from South Asia with two further South Asian clades of moderate resistance. Greenhouse bioassays indicated that planthoppers can develop virulence against multiple resistance genes including genes introgressed from wild rice species. Nilaparvata lugens populations from Punjab (India) and the Mekong Delta (Vietnam) were highly virulent to a range of key resistance donors irrespective of variety origin. Sogatella furcifera populations were less virulent to donors than N. lugens; however, several genes for resistance to S. furcifera are now ineffective in East Asia. A clade of International Rice Research Institute (IRRI)-bred varieties and breeding lines, without identified leafhopper-resistance genes, were highly resistant to the green leafhopper, Nephotettix virescens. Routine phenotyping during breeding programs likely maintains high levels of

Temperature-dependent oviposition and nymph performance reveal distinct thermal niches of coexisting planthoppers with similar thresholds for development

“…We used the laboratory colonies because they were free of associated plant viruses and had largely synchronized development stages. The BPH colony had noted virulence against a range of resistance genes including BPH1, BPH2, BPH5, BPH7, BPH8, BPH18, BPH25 and BPH26 and displayed a high level of brachyptery [62]. The WBPH PLOS ONE colony had noted virulence against Wbph2, Wbph3, wbph4, Wbph6, WbphAR, WbphM1 and WbphM2 [62].…”

“…The BPH colony had noted virulence against a range of resistance genes including BPH1, BPH2, BPH5, BPH7, BPH8, BPH18, BPH25 and BPH26 and displayed a high level of brachyptery [62]. The WBPH PLOS ONE colony had noted virulence against Wbph2, Wbph3, wbph4, Wbph6, WbphAR, WbphM1 and WbphM2 [62]. The planthoppers were reared continuously on the susceptible variety TN1 (� 30-day old rice plants) in wire mesh cages (91.5 × 56.5 × 56.5 cm; H × L × W).…”

Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance

“…Pyramiding resistance genes against phloem-feeding herbivores is largely a response to the rapid adaptation by planthoppers and leafhoppers to resistant rice varieties ( Bottrell and Schoenly, 2012 ; Horgan and Crisol, 2013 ; Horgan, 2018 ). The first monogenic resistant varieties released in Asia during the 1970s and 1980s were overcome by planthoppers in as little as 2 years (12 generations), but several traditional varieties with polygenic resistance have continued to be highly resistant to leafhoppers and planthoppers in screening studies (e.g., PTB33, Rathu Heenati: Horgan et al, 2015 , 2017 ). In our study, leafhoppers adapted to feed on GRH2/GRH4- PYL within 5–10 generations and to oviposit on GRH2/GRH4- PYL within 20 generations.…”

“…These individuals may possess virulence genes that are closely associated with specific resistance genes (i.e., Jing et al, 2014 ; Kobayashi et al, 2014 ). Because virulence against ≥2 genes is common among planthoppers and leafhoppers ( Myint et al, 2009a , 2009b ; Horgan et al, 2015 , 2017 ), forerunners with several virulence genes may also exist, although at lower frequencies ( Horgan, 2018 ). Furthermore, planthoppers (and possibly leafhoppers) that overcome one gene, will often gain virulence to other, unrelated genes (e.g., BPH8 and BPH9 : Ketipearachchi et al, 1998 ; BPH3/BPH32 and BPH4 : Peñalver Cruz et al, 2011 ).…”

Unanticipated benefits and potential ecological costs associated with pyramiding leafhopper resistance loci in rice

“…Ecological theory suggests that strong resistance is also likely to have associated costs as plants must balance growth, reproduction and defence (including maintenance) to achieve optimal life-history strategies in their respective niches ( Herms and Mattson, 1992 ; Horgan et al, 2009 ). Research on traditional rice varieties with polygenic herbivore resistance supports many of these ideas ( Hirae et al, 2007 ; Horgan et al, 2015 , 2017 ). However, despite the tremendous investments into pyramiding herbivore resistance genes/loci, surprisingly few researchers have tested these hypotheses using available near-isogenic materials.…”