Inoculation of cucumber plants with Beauveria bassiana enhances resistance to Aphis gossypii (Hemiptera: Aphididae) and increases aphid susceptibility to pirimicarb

Abstract

The entomopathogen Beauveria bassiana (Bals.) Vuill. (Ascomycota: Hypocreales) can colonize plants endophytically and stimulate the production of secondary plant metabolites with anti-herbivore activities. We assayed the topical virulence of B. bassiana to Aphis gossypii Glover (Hemiptera: Aphididae), the effects of cucumber inoculation with this fungus on plant metabolites, and the physiological consequences for aphids that fed on these plants. Assays were conducted with both the commercial formulation of B. bassiana, 'Naturalis®-L', at the recommended concentration of 1.5 ml / L (yielding a spore concentration of 2.3 × 107 CFU per ml), and with a similar concentration of the isolated fungal strain. Topical application of 0.03 ml of solution per cm2, or 1 × 103 CFU, caused 100% mortality to A. gossypii adults after seven days, whether Naturalis®-L or the isolate alone was used. The fungus grew endophytically into foliage when sprayed on cucumbers at the 2-leaf stage and concentrations of alkaloids, flavonoids, phenols, hydrogen peroxide, and total chlorophyll were higher than in control plants 28 days after inoculation. Malondialdehyde content, plant growth, and total yield were unaffected by B. bassiana inoculation. Aphids fed on B. bassiana-inoculated plants for 24 h had reduced activities of detoxifying enzymes (glutathione-S-transferase, carboxylesterase, and acetylcholinesterase) compared to controls. Activities of digestive enzymes, (lipase, α-amylase, α-glucosidase, and aminopeptidase) were reduced in aphids from inoculated plants, which exhibited higher activities of superoxide dismutase, ascorbate peroxidase, and phenoloxidase, but lower catalase activity. Energy reserves (lipids, protein, and glycogen) were lower in aphids from inoculated plants, and they exhibited reduced fecundity, longevity, and reproductive periods, and a 50% reduction in the LC50 of pirimicarb. Thus, in addition to causing direct pathogenicity, inoculation of plants with B. bassiana negatively impacted A. gossypii physiology and reproductive performance and could usefully complement other strategies for managing cotton aphids on greenhouse cucumber.