A snapshot of the transcriptome of Medicago truncatula (Fabales: Fabaceae) shoots and roots in response to an arbuscular mycorrhizal fungus and the pea aphid (Acyrthosiphon pisum) (Hemiptera: Aphididae).

Plants simultaneously interact with belowground symbionts such as arbuscular mycorrhizal (AM) fungi and aboveground antagonists such as aphids. Generally, plants gain access to valuable resources including nutrients and water through the AM symbiosis and are more resistant to pests. Nevertheless, aphids' performance improves on mycorrhizal plants, and it remains unclear whether a more nutritious food source and/or attenuated defenses are the contributing factors. This study examined the shoot and root transcriptome of barrel medic (Medicago truncatula Gaertn.) plants highly colonized by the AM fungus Rhizophagus irregularis (Blaszk., Wubet, Renker, and Buscot) C. Walker and A. Schüßler (Glomerales: Glomeraceae) and exposed to 7 days of mixed age pea aphid (Acyrthosiphon pisum (Harris)) herbivory. The RNA-seq samples chosen for this study showed that aphids were heavier when fed mycorrhizal plants compared to nonmycorrhizal plants. We hypothesized that (i) insect-related plant defense pathways will be downregulated in shoots of mycorrhizal plants with aphids compared to nonmycorrhizal plants with aphids; (ii) pathways involved in nutrient acquisition, carbohydrate-related and amino acid transport will be upregulated in shoots of mycorrhizal plants with aphids compared to nonmycorrhizal plants with aphids; and (iii) roots of mycorrhizal plants with aphids will exhibit mycorrhiza-induced resistance. The transcriptome data revealed that the gene repertoire related to defenses, nutrient transport, and carbohydrates differs between nonmycorrhizal and mycorrhizal plants with aphids, which could explain the weight gain in aphids. We also identified novel candidate genes that are differentially expressed in nonmycorrhizal plants with aphids, thus setting the stage for future functional studies.

Priming Seeds with Indole and (Z)-3-Hexenyl Acetate Enhances Resistance Against Herbivores and Stimulates Growth.

A striking feature of plant ecology is the ability of plants to detect and respond to environmental cues such as herbivore-induced plant volatiles (HIPVs) by priming or directly activating defenses against future herbivores. However, whether seeds also respond to compounds that are common constituents of HIPV blends and initiate future plant resistance is unknown. Considering that seeds depend on other environmental cues to determine basic survival traits such as germination timing, we predicted that seeds exposed to synthetic constituents of HIPV blends would generate well-defended plants. We investigated the effect of seed exposure to common volatiles on growth, reproduction, and resistance characteristics in the model plants Arabidopsis thaliana and Medicago truncatula using herbivores from two feeding guilds. After seed scarification and vernalization, we treated seeds with one of seven different plant-derived volatile compounds for 24 h. Seeds were then germinated and the resulting plants were assayed for growth, herbivore resistance, and expression of inducible defense genes. Of all the synthetic volatiles tested, indole specifically reduced both beet armyworm growth on A. thaliana and pea aphid fecundity on M. truncatula. The induction of defense genes was not affected by seed exposure to indole in either plant species, indicating that activation of direct resistance rather than inducible resistance is the mechanism by which seed priming operates. Moreover, neither plant species showed any negative effect of seed exposure to any synthetic volatile on vegetative and reproductive growth. Rather, M. truncatula plants derived from seeds exposed to (Z)-3-hexanol and (Z)-3-hexenyl acetate grew larger compared to controls. Our results indicate that seeds are sensitive to specific volatiles in ways that enhance resistance profiles with no apparent costs in terms of growth. Seed priming by HIPVs may represent a novel ecological mechanism of plant-to-plant interactions, with broad potential applications in agriculture and seed conservation.