Mutualism promotes insect fitness by fungal nutrient compensation and facilitates fungus propagation by mediating insect oviposition preference

Abstract

Penicillium and Bactrocera dorsalis (oriental fruit fly, Hendel) are major pathogens and pests of citrus fruits, as both of them can cause detrimental losses in citrus production. However, their interaction in the cohabitation of citrus fruits remains elusive. In this study, we revealed a mutualistic relationship between Penicillium and B. dorsalis. We found that insect behaviors can facilitate the entry of fungal pathogens into fruits, and fungal pathogens promote the fitness of insects in return. More specifically, Penicillium could take advantage of the openings left by ovipositors of flies, and adult flies contaminated with Penicillium could spread the fungus to new sites. Moreover, the volatile emissions from fungi could attract gravid flies to the infected site for egg laying. The fungus and B. dorsalis were able to establish mutual interaction, as revealed by the presence of Penicillium DNA in intestinal tracts of flies throughout all larval stages. The fungal partner seemed to promote the emergence rate and shorten the emergence duration of the flies by providing pyridoxine, one of the B group vitamins. Different from previously reported scenarios of strong avoidance of Drosophila and attraction of Aedes aegypti toward Penicillium, our findings unveil a hitherto new paradigm of the mutualism between Penicillium and B. dorsalis, by which both insect and fungus earn benefits to facilitate their propagation.

The modulatory effects of biogenic amines on male mating performance in Bactrocera dorsalis

“…Adult flies were reared on artificial diets consisting of yeast extract (25%) and sugar (75%). Larval diets consist of banana (31.8%), corn (31.8%), yeast extract (3.2%), sugar (3.2%), sodium benzoate (0.1%), fiber (paper towel, 3.2%), hydrochloric acid (0.2%) and distilled water (26.5%) ( Gu et al, 2022 ).…”

Anti-Insect Properties of Penicillium Secondary Metabolites

“…Gravid females of the oriental fruit fly ( Bactrocera dorsalis : Diptera, Tephritidae) were found to be attracted by VOCs emitted by a strain of P. citrinum . After finding the fungus in the intestinal tracts throughout all larval stages, a mutualistic association between the two organisms based on nutritional supplementation was postulated, which could be considered a possible target in control programs [ 229 ]. Likewise, three Penicillium species, namely P. citrinum , P. sumatrense , and P. digitatum , were found to influence the oviposition selection and behavior of the yellow peach moth ( Conogethes punctiferalis : Lepidoptera, Crambidae).…”

Penicillium-Infected Apples Benefit Larval Development of Conogethes punctiferalis via Alterations of Their Gut Bacteria Community and Gene Expression

“…Consequently, insects may satisfy their nutritional requirements by directly consuming microorganisms or their metabolic byproducts . Moreover, microbial infection of plants can alter their volatile compound composition, thereby influencing the oviposition behavior of mated female insects to exhibit avoidance or preference. , Furthermore, plant pathogens can indirectly impact the feeding behavior of herbivorous insects by modulating the content, composition, and yield of host plant secondary metabolites. , For instance, spotted-wing Drosophila exhibit avoidance behavior toward cranberry fruits infected with gray mold pathogen Botrytis cinerea; oriental fruit fly Bactrocera dorsalis infected with Penicillium can provide the nutritional compound pyridoxine, one of the B group vitamins to promote the growth and development of young fruit fly larvae . Therefore, plant pathogens play a crucial role in regulating the interactions between insects and plants.…”

“…3,5 For instance, spotted-wing Drosophila exhibit avoidance behavior toward cranberry fruits infected with gray mold pathogen Botrytis cinerea; 6 oriental fruit fly Bactrocera dorsalis infected with Penicillium can provide the nutritional compound pyridoxine, one of the B group vitamins to promote the growth and development of young fruit fly larvae. 7 Therefore, plant pathogens play a crucial role in regulating the interactions between insects and plants. Their involvement renders the interaction between host plants and herbivorous insects more intricate, resulting in changes in the host plant preference and adaptation of the herbivorous insects.…”