Evolving ideas about genetics underlying insect virulence to plant resistance in rice-brown planthopper interactions

Highlights

• Genetic studies of BPH virulence to rice resistance are reviewed.

• Heterogeneity in BPH ’biotypes’ can cause unreliable analyses results.

• Some BPH host adaptations to rice resistance have gene-for-gene relationships.

Abstract

Many plant-parasite interactions that include major plant resistance genes have subsequently been shown to exhibit features of gene-for-gene interactions between plant Resistance genes and parasite Avirulence genes. The brown planthopper (BPH) Nilaparvata lugens is an important pest of rice (Oryza sativa). Historically, major Resistance genes have played an important role in agriculture. As is common in gene-for-gene interactions, evolution of BPH virulence compromises the effectiveness of singly-deployed resistance genes. It is therefore surprising that laboratory studies of BPH have supported the conclusion that virulence is conferred by changes in many genes rather than a change in a single gene, as is proposed by the gene-for-gene model. Here we review the behaviour, physiology and genetics of the BPH in the context of host plant resistance. A problem for genetic understanding has been the use of various insect populations that differ in frequencies of virulent genotypes. We show that the previously proposed polygenic inheritance of BPH virulence can be explained by the heterogeneity of parental populations. Genetic mapping of Avirulence genes indicates that virulence is a monogenic trait. These evolving concepts, which have brought the gene-for-gene model back into the picture, are accelerating our understanding of rice-BPH interactions at the molecular level.

Introduction

The brown planthopper (BPH), Nilaparvata lugens (Stål) (Homoptera: Delphacidae) is distributed throughout regions of South Asia, South East Asia and East Asia where rice (Oryza sativa) is grown, and is one of the most destructive insect pests of rice (Sogawa, 1982). Resistant rice varieties carrying either major genes or quantitative trait loci (QTLs) associated with resistance are widely used to control this pest (Fujita et al., 2013, Jena and Kim, 2010). In spite of the deployment of resistant varieties, the BPH continues to be an important pest. Rapid population growth on modern high-yield rice varieties, and the loss of natural enemies owing to the misuse of insecticides are two important problems. Another is the evolution of virulent BPH populations that survive on resistant rice varieties (Gallagher et al., 1994, Kenmore et al., 1984, Sogawa, 2014). Evolution of BPH virulence is currently the main obstacle for successful breeding and deployment of BPH-resistant rice.

Most BPH-resistant rice varieties possess major resistance genes that are associated with inhibition of feeding and reductions in growth rate, longevity and fecundity (Fujita et al., 2013, Horgan, 2009, Sogawa, 1982, Sogawa and Pathak, 1970). To date, three of these genes, Bph14 (Du et al., 2009), BPH26 (Tamura et al., 2014) and Bph3 (Liu et al., 2015) have been identified. Bph14 and BPH26 are associated with inhibition of feeding and both encode proteins containing coiled-coil (CC)-nuclear binding site (NBS)-leucine rich repeat (LRR) motifs (Du et al., 2009, Tamura et al., 2014). Plants often use a CC–NBS–LRR protein as a surveillance system or sentry that triggers effector-triggered immunity (ETI) after perceiving an effector, encoded by a cognate Avirulence gene (Spoel and Dong, 2012). Many plant parasites, including insects, introduce effectors onto or into plant cells in order to suppress plant defense and/or manipulate the plant to produce more food or a different food (Harris et al., 2015). Taken together, this evidence suggests that BPH, like plant pathogens and other insects like the Hessian fly, use effector proteins throughout colonization and sustained feeding. It also suggests that rice Resistance (R) proteins may interact with BPH effectors in a gene-for-gene manner, in which each R protein perceives, directly or indirectly, an effector encoded by a specific BPH Avirulence (Avr) gene (Fig. 1; Cheng et al., 2013, Flor, 1971, Harris et al., 2015, Thompson and Burdon, 1992). The plant-parasite R gene-Avr gene interaction that underlies ETI has been thoroughly examined in many plant-bacteria, plant-fungus, and plant-oomycete interactions (Cui et al., 2015). Recent reviews have stressed that effectors are also important in the lives of insects (Bos et al., 2010, Hogenhout et al., 2009). Just last year, thirty years after the cloning of the first plant pathogen Avirulence gene (Staskawicz et al., 1984), the first insect Avirulence gene, vH13, was cloned in the Hessian fly, Mayetiola destructor (Aggarwal et al., 2014), a well-known pest of wheat whose gene-for-gene interactions have been studied for over 50 years. Since then, two other Hessian fly Avirulence genes have been cloned, the vH9 published in the report of the genome sequence of the Hessian fly (Zhao et al., 2015a), and vH24 reported in this Special Issue (Zhao et al., 2016). Progress towards understanding gene-for-gene interactions has also been made for another rice pest, the Asian rice gall midge (Orseolia oryzae) (Bentur et al., 2016). Recent reviews (Chen et al., 2012, Cheng et al., 2013, Lou et al., 2014) support the idea that BPH resembles these other two parasites of grasses (Harris et al., 2003) in showing features of gene-for-gene interactions, as well as features of the plant reprogramming that is the subject of this Special Issue. It also raises the question of interesting similarities with plant pathogens, which in the Hessian fly inspired the title of a recent review “Gall Midges (Hessian fly) as Plant Pathogens” (Stuart et al., 2012).

Here, I review the progress towards understanding resistance in rice and virulence in BPH. Although studies of BPH physiology, behaviour and genetics have not identified the main factors that determine how the BPH overcomes host resistance, studies using BPH ‘biotypes’ (populations that have adapted to specific rice resistance genotypes, Table 1) have shown that virulence to different BPH-resistance genes overlaps between ‘biotypes’. These studies concluded that adaptation to plant resistance is conferred by changes in many genes, i.e., it is a polygenic trait rather than a monogenic trait conferred by a change(s) in a single gene, as proposed by the gene-for-gene model (Claridge and Den Hollander, 1982, Claridge and Den Hollander, 1983, Den Hollander and Pathak, 1981, Diehl and Bush, 1984, Roderick, 1994, Sogawa, 1982, Tanaka, 1999). Clearly, a large gap remains in our understanding of the gene-for-gene concept of rice and the BPH. Progress in the understanding of genetic diversity in geographic populations based on population genetics, and the mechanisms resulting in changes in frequency in virulence in BPH populations have steadily refined our understanding of BPH ‘biotypes’ (Claridge and Den Hollander, 1982, Diehl and Bush, 1984, Downie, 2010, Khan and Saxena, 1990, Roderick, 1994, Roderick, 1996, Thompson and Burdon, 1992). Laboratory experiments using new molecular biology technologies and tools have led to an understanding of the genetic mechanisms of BPH virulence (Jairin et al., 2013, Jing et al., 2014, Kobayashi et al., 2014). In addition, the release of the BPH genome sequence promises significant advances in the molecular interactions of host-plant resistance (Xue et al., 2014). This review focuses on the development of virulent BPH populations, genetics of virulence to rice resistance in relation to the genetic diversity in these populations, and the importance of considering the genetic background of insect populations used in studies of host-parasite interactions.