Hessian fly Avirulence gene loss‐of‐function defeats plant resistance without compromising the larva's ability to induce a gall tissue

Abstract

Plant pathogen effectors encoded by Avirulence (Avr) genes benefit the pathogen by promoting colonization and benefit plants that have a matching resistance (R) gene by constituting a signal that triggers resistance. The Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae), resembles a plant pathogen in showing R/Avr interactions. Because of these interactions, a wheat plant with the H13 resistance gene can be resistant or susceptible depending on the genotype of the larva that attacks the plant, being resistant if attack comes from a larva with a functional vH13 gene, but susceptible if attack comes from a larva with a non‐functional vH13 gene. In this study we asked: does this susceptible interaction involving plants with H13 look like susceptible interactions with plants lacking H13? Possibly, the H13 plant attacked by a larva with a non‐functional vH13 is induced to partial rather than complete resistance. Or the larva, lacking its vH13‐encoded effector, is compromised in its ability to induce susceptibility, which includes forcing the plant to create a gall nutritive tissue. Responses of epidermal cells to larval attack were explored using imaging techniques (light microscopy, scanning and transmission electron microscopy). Whole‐organism responses were investigated by measuring the growth of plants and larvae. No evidence was found for partial resistance responses by H13 plants or for a compromise in the ability of vH13 loss‐of‐function larvae to induce susceptibility. It appears that disrupting vH13 function is sufficient for overcoming the induced resistance mediated by the H13 gene.

The adult head morphology of the hessian flyMayetiola destructor(diptera, cecidomyiidae)

“…After enclosing from the egg, the tiny larva (<0.5 mm) attacks undifferentiated plant cells found in zones of active growth (e.g., buds, expanding leaves). Effectors produced in the larva's extremely large salivary glands (Stuart and Hatchett, 1987; Stuart et al, ), in conjunction with specialized attack behavior (Rohfrisch, ), allow the larva to manipulate the developmental pathway of plant cells, creating a “nutritive” tissue that provides an enriched diet for the larva at the expense of plant growth (Harris et al, ). Often associated with the microscopic nutritive tissue is a macroscopic gall, which comes in a wide variety of forms (Gagné, ).…”

Implementing an evolutionary framework for understanding genetic relationships of phenotypically defined insect biotypes in the invasive soybean aphid (Aphis glycines)

“…Biotypic virulence is commonly explained via the gene‐for‐gene model, in which plant resistance and biotypic dynamics are characterized by interactions between gene pairings within the interacting species (Smith and Boyko ; Harris et al. ; Smith and Clement ). Aphids are known to produce effectors, small proteins that modulate plant host cell and defense processes (Hogenhout et al.…”

“…Thus, virulence traits could have pre-existed within the invasive population and then became widely dispersed. Biotypic virulence is commonly explained via the genefor-gene model, in which plant resistance and biotypic dynamics are characterized by interactions between gene pairings within the interacting species (Smith and Boyko 2007;Harris et al 2012;Smith and Clement 2012). Aphids are known to produce effectors, small proteins that modulate plant host cell and defense processes (Hogenhout et al 2009;Bos et al 2010), which may provide genetic machinery for such a gene-for-gene response.…”

Pivoting from Arabidopsis to wheat to understand how agricultural plants integrate responses to biotic stress

“…This is where the first-instar larva sits sucking up fluids (Refai et al, 1956). There is a clear association between plant growth deficits and the induced nutritive tissue (Table 2; Harris et al, 2012). This is common for gall inducers, which reprogramme source-sink relationships within the plant, the result being insect growth at the expense of plant growth (Larson and Whitham, 1991).…”

“…In the case of the Hessian fly, plant growth effects do not appear to be density dependent. A single larva is sufficient to induce stunting of the plant (Berzonsky et al, 2003;Harris et al, 2012).…”