Resistance and susceptibility in interactions between apple and woolly aphids

 Reference: CTP_FCR_2019_6

This student is to be registered with the Harper Adams University.

Lead academic supervisors: Ms Felicidad Fernández and Dr Glen Powell, NIAB EMR
University supervisors: Dr Tom Pope and Dr Simon Segar, Harper Adams University


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; Er4 on chromosome 7. 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 the 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, 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. The genetic diversity and genetic population structure of E. lanigerum has been investigated using microsatellite molecular markers in China and Chile, 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. 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.


The specific research objectives of the project include:

  • 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.
  • Characterise the ecology and life cycle of WAA in the UK.
  • Assess responses of different WAA clonal genotypes to key aphid resistance genes in apple.
  • Elucidate the inheritance of resistance from novel sources and determine interactions or linkage with currently described genes.
  • Identify candidate genes and propose mechanisms for apple resistance to WAA.
  • 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.


These objectives will be achieved by:

  • Application of molecular markers to provide an unprecedented analysis of WAA genetic diversity in the UK using samples from growers’ sites. Use of these markers to compare UK WAA genetic diversity with aphid strains provided by collaborators overseas, including New Zealand and South Africa where there is well established evidence of resistance-breaking aphid genotypes (Year 1).
  • Investigations of the aphid life cycle and potential to produce sexual forms and lay viable eggs, including field sampling of colonies in orchards. These studies will also include transfer of laboratory-reared clones to short-day environmental cabinets, mimicking the autumnal conditions inducing sexual forms to explore whether UK genotypes of the aphid are capable of sexual reproduction (Years 1 & 2).
  • Rearing multiple aphid genotypes collected from different locations, testing these clones for performance (glasshouse-based bioassays of survival and reproduction) on apple accessions with key resistance alleles; comparisons with susceptible accessions to identify relatively virulent and avirulent pest clones (Years 2 & 3).
  • Development and application of DNA markers to refine map positions for Er1 and Er2 resistance genes and identify putative resistance genes using the apple genome and ongoing annotations from the GDR collaborative programmes (Year 1)
  • Study the inheritance of WAA resistance in progenies derived from other novel sources of aphid resistance, map resistance genes and identify putative resistance genes (as above) (Years 2 – 4)
  • Investigate possible effects of secondary genes in progeny segregations (Years 2 – 4)
  • Testing the most virulent aphid genotypes identified in Years 1-3 on apple lines with multiple resistance alleles, helping to identify accessions with the greatest potential for future breeding programmes (Year 4

    Applying for this studentship

    The most important eligibility criterion for this funded studentship is residency:

    1. UK students: If you have been ordinarily resident in the UK for three years you will normally be entitled to apply for a full studentship, covering tuition fees and a maintenance stipend.
    2. EU students: If you have been ordinarily resident in another EU country (outside the UK) for three years you will normally be able to apply for a tuition fees-only award (without a maintenance stipend). If you have lived in the UK for three years you may be eligible for a full studentship.

This eligibility is unaffected by Brexit. The UK Government has guaranteed EU eligibility for Research Council funding for PhDs beginning before the end of the 2019-20 academic year.

Anyone interested should contact for an application form and return the form to before the deadline of 28th February 2019.