Inbreeding, herbivory, and the transcriptome of Solanum carolinense

Abstract

Both inbreeding and herbivory are common in flowering plants, and both are known to reduce fitness. Although inbreeding might also be expected to impact inducible and constitutive plant defenses against herbivores in a variety of ways, investigators have only recently begun to examine the effects of inbreeding on resistance to herbivores. Here, we examined the effects of inbreeding in horsenettle, Solanum carolinense L. (Solanaceae), on herbivore damage and reproductive output under field conditions. In addition, we employed the commercially available Affymetrix tomato (Solanum esculentum L.) microarray to explore changes in S. carolinense gene expression associated with feeding by Manduca sexta) (L.) (Lepidoptera: Sphingidae) caterpillars on inbred and outbred horsenettle plants. We found that the inbred horsenettle plants experienced significantly greater herbivore damage in the field and exhibited only 11% of the seed production of outbred plants. Flea beetles and false potato beetles were the most abundant herbivores observed on the experimental plants, and both were observed significantly more often on inbred plants. The microarray‐generated transcriptomes of horsenettle revealed that the commercially available microarray chips can be reliably used with this important weed, that damage significantly up‐regulates many defense‐related genes, and that inbreeding depresses the expression of many genes especially those located in the jasmonic acid, ethylene, abscisic acid, and systemin‐mediated pathways that regulate the induction of defensive compounds and organic volatiles. Findings of the field study and the gene‐expression analysis are thus complementary, as the former demonstrates that inbreeding impacts plant resistance to herbivores, whereas the latter provides initial insights into the genetic mechanisms underlying these effects and their relationship to fitness.

Landscape alteration and habitat modification: impacts on plant–pollinator systems

“…Recent work using experimentally inbred plant lines has shown that inbreeding depressed gene expression in pathways (e.g. jasmonic acid and ethylene) that regulate the induction of defensive compounds and organic volatiles [70]. This altered trophic interactions with inbred plants emitting more constitutive volatiles, which attracted greater numbers of herbivores, but fewer herbivore-induced volatiles leading to reduced natural enemy recruitment [68 ].…”

Inbreeding in horsenettle (Solanum carolinense) alters night-time volatile emissions that guide oviposition byManduca sextamoths

“…Given the strong possibility that disruption of terpene production and/or storage is related to the behavioural patterns we have observed, future work should focus on understanding how inbreeding disrupts the production of terpene synthase enzymes and other constitutive chemical and physical defences (e.g. transcriptome analysis), a task that is now feasible owing to the recent successful hybridization of horsenettle transcripts with commercially available tomato microarray chips [49].…”

Inbreeding compromises host plant defense gene expression and improves herbivore survival

“…This hypothesis is supported by a preliminary microarray study comparing the response of inbred and outbred herbivore damaged horsenettle genets-which revealed that the jasmonic acid (JA) pathway (a key biochemical pathway employed to defend against chewing herbivores such as M. sexta) was compromised due to inbreeding. 18 Results from Kariyat et al 18 suggest that variation in the gene expression levels of plant produced defense compounds, due to inbreeding, could be responsible for changes to growth, 15 oviposition, 14 and flight capacity 15 of M. sexta. However, no studies have directly compared relative expression levels (RA) of genes in the JA pathway between inbred and outbred horsenettle plants, or linked differences in defense gene RAs, due to inbreeding, to changes in herbivore performance.…”

“…26,15 It also might explain why inbred plants are preferred in choice experiments by both M. sexta larvae 12,10 and ovipositing females. 14 Inbreeding in horsenettle causes significant reductions in the plant's induced defense responses 18,23 and resistance to herbivory. [8][9][10] We used only minimal manipulation, a single generation of host plant inbreeding, to produce differences (inbred vs. outbred) in the host plants of an indigenous plant-insect system (horsenettle-tobacco hornworm).…”

“…This trend is supported by a microarray study that showed herbivore damaged inbred horsenettle plants exhibited a 2 fold decrease in expression levels of gene clusters related to herbivore defense. 18 In addition to the pivotal role that JA plays in plant direct chemical defense, JA is also involved in the synthesis of plant volatiles, a major element of indirect defense. Previous field trials, using M. sexta damaged horsenettle plants, showed that inbreeding curtails the plant's production of key terpenoid volatiles 24 -this negatively impacts the plant's ability to attract predators and/or parasitoids.…”