Resistance and susceptibility in interactions between apple and woolly aphids

Abstract

Objectives The specific research objectives of the project include: 1) Investigate the genetic diversity of UK populations of WAA and compare with diversity within this aphid species in other regions of the world using a combined SSR and population genomic approach. 2) Characterise the ecology and life cycle of WAA in the UK. 3) Assess responses of different WAA clonal genotypes to key aphid resistance genes in apple. 4) Elucidate the inheritance of resistance from novel sources and determine interactions or linkage with currently described genes. 5) Identify candidate genes and propose mechanisms for apple resistance to WAA. 6) Characterise aphid resistance loci in apple accessions and determine the effect of pyramided resistance genes on resistance-breaking aphid genotypes, highlighting accessions with potential for use in future breeding programmes.

Description

The woolly apple aphid (WAA; Eriosoma lanigerum) is one of the most important pests of apples in many of the world’s apple-growing regions, able to feed from the roots, trunks, branches and shoots. The insects secrete long white waxy filaments that form a woolly covering providing protection to the colony. The injection of saliva by the aphids distorts plant growth, causing the development of nodules and cracking of bark. The honeydew that is produced by large colonies further damages the tree by encouraging the growth of sooty moulds. WAA has been considered a sporadic pest of UK apple production, but infestations have increased following the recent withdrawal of two effective insecticides (chlorpyrifos and pirimicarb), leading to significant risks of fruit rejections. Globally, WAA is one of the most devastating apple orchard pests, particularly in hot climates such as South Africa and Australia where severe infestations of the root system frequently compromise tree survival, especially in young plantings. Breeding of resistant rootstocks is increasingly critical for orchard longevity but the molecular mechanisms underpinning this resistance and the effects of pyramiding multiple resistance genes are not fully understood. There have been multiple sources of resistance identified but not all are equally well characterised with regards to their position in the genome or inheritance. Four sources of resistance have been described as major single Eriosoma resistance (Er) genes and tentatively mapped: Er1 and Er3 at the top of chromosome 8 (close to each other but considered distinct based on differential response to resistance breaking isolates in New Zealand); Er2 at the top of chromosome 17 (Bus et al., 2008); Er4 on chromosome 7 (Bus et al., 2010). However, significant segregation distortions in the inheritance of the trait raises further questions about linked deleterious genes and secondary genes involved in the plant response. Woolly apple aphid susceptibility has traditionally been considered a qualitative trait with plants being categorised as either susceptible or resistant, but intensity of infestation on susceptible plant material varies greatly. Additionally, resistance breaking genotypes of WAA have been reported for Er1, Er2 and Er3. Er1-resistance breaking clones are progressively becoming a serious problem in some regions, in particular in South Africa. An understanding, therefore, of the mechanism(s) of resistance and the identification of tightly linked markers to allow for gene pyramiding is urgent. Furthermore, there is a lack of knowledge concerning the life cycle and genetic diversity of the pest. The aphid reproduces asexually (by parthenogenesis) and there may be up to 20 generations in a year. Overwintering usually occurs as asexual juvenile stages (nymphs) hidden away in cracks in the tree bark or feeding on roots. However, sexual forms are sometimes produced in autumn and sexual females then lay eggs for overwintering. In many parts of the world, including the UK, it has been proposed that the aphids that hatch from these sexually-produced eggs die without feeding (Blackman & Eastop, 2000), and the population may therefore be functionally asexual. However, studies of the genetic structure of such populations have not been carried out, and it is possible that successful sexual reproduction does occasionally occur on apple, as has been recorded elsewhere (e.g. Sandanayaka & Bus, 2005). The genetic diversity and genetic population structure of E. lanigerum has been investigated using microsatellite molecular markers in China (Zhou et al., 2015) and Chile (Lavandero et al., 2011), but, despite uncertainty regarding the sexual or asexual nature of the lifecycle, the aphid’s genetic diversity has not been investigated in the UK. Sexual reproduction in aphids may lead to the rapid emergence of new clones with increased virulence on plants that were previously resistant to the pest (Kanvil et al., 2014). A better understanding of the pest’s life cycle and genetic population structure is therefore critical to help inform effective plant breeding strategies. NIAB EMR has recently detected the presence of resistance-breaking biotypes of WAA in glasshouse screening experiments carried out as part of the apple breeding programme. Colonies were found on rootstocks carrying both Er1 and Er2 resistance alleles. This could have serious implications for infestation levels of WAA in UK orchards, making this pest a priority in a warming climate. This studentship presents an exciting training opportunity to address the current lack of knowledge concerning plant resistance to WAA and the life cycle and genetic diversity of the pest. The student will work alongside recognised research scientists and colleagues from industry (growers and agronomists) to develop skills in plant and insect science that will help address practical aspects of agronomy and food security. The project will provide training in important scientific skills including development and application of molecular markers, screening plants for resistance to insects, studying insect ecology in the field and using environmentally-controlled cabinets to mimic seasonal changes in temperature and day-length to explore the pest’s life-cycle responses.