Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense

• Published in: PloS one 2022-10, Vol.17 (10), p.e0274920
• Main Authors: Nihranz, Chad T, Helms, Anjel M, Tooker, John F, Mescher, Mark C, De Moraes, Consuelo M, Stephenson, Andrew G
• Format: Article
• Language: English
• Subjects: Analysis; Biology and Life Sciences; Caterpillars; Chemical defense; Control; Damage; Diseases and pests; Ecology and Environmental Sciences; Emissions; Environmental aspects; Epigenetic inheritance; Genetic crosses; Growth; Health aspects; Herbivores; Herbivory; Identification and classification; Inbreeding; Methods; Offspring; Organic compounds; Pest resistance; Phenotype; Phenotypes; Physical Sciences; Phytophagous insects; Plant Leaves; Plants; Seeds; Side effects; Solanaceae; Solanum - chemistry; Solanum carolinense; Spine; Transgenic plants; Trichomes; VOCs; Volatile organic compounds; Volatile Organic Compounds - metabolism
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0274920

In addition to directly inducing physical and chemical defenses, herbivory experienced by plants in one generation can influence the expression of defensive traits in offspring. Plant defense phenotypes can be compromised by inbreeding, and there is some evidence that such adverse effects can extend to the transgenerational expression of induced resistance. We explored how the inbreeding status of maternal Solanum carolinense plants influenced the transgenerational effects of herbivory on the defensive traits and herbivore resistance of offspring. Manduca sexta caterpillars were used to damage inbred and outbred S. carolinense maternal plants and cross pollinations were performed to produced seeds from herbivore-damaged and undamaged, inbred and outbred maternal plants. Seeds were grown in the greenhouse to assess offspring defense-related traits (i.e., leaf trichomes, internode spines, volatile organic compounds) and resistance to herbivores. We found that feeding by M. sexta caterpillars on maternal plants had a positive influence on trichome and spine production in offspring and that caterpillar development on offspring of herbivore-damaged maternal plants was delayed relative to that on offspring of undamaged plants. Offspring of inbred maternal plants had reduced spine production, compared to those of outbred maternal plants, and caterpillars performed better on the offspring of inbred plants. Both herbivory and inbreeding in the maternal generation altered volatile emissions of offspring. In general, maternal plant inbreeding dampened transgenerational effects of herbivory on offspring defensive traits and herbivore resistance. Taken together, this study demonstrates that inducible defenses in S. carolinense can persist across generations and that inbreeding compromises transgenerational resistance in S. carolinense.