A herbivore-induced plant volatile primes seeds for long-term anti-herbivore defense

Background/Question/Methods

Herbivore-induced plant volatiles (HIPVs) play a crucial role in facilitating plant ecological interactions above and below ground, including priming plants for future stress. Seeds may lay dormant for years in the soil and are likely exposed to an array of HIPVs, either through direct exposure or through leaching. Such exposure may affect the growth, development, and defense profiles when the seeds grow into mature plants. Despite the ecological relevance, the long-term effects of seed exposure to HIPVs on growth and defenses of future plants are unknown. We exposed seeds of two model species, Arabidopsis thaliana and Medicago truncatula, to five individual HIPVs (cis-3-hexenol, cis-3-hexenyl acetate, trans-2-hexenal, β-caryophyllene and indole) in growth chamber and greenhouse experiments. We examined the effects of seed exposure to HIPVs on plant growth and anti-herbivore defense against either a chewing herbivore (beet armyworm; Spodoptera exigua) or a phloem-feeding herbivore (pea aphid; Acyrthosiphon pisum). We measured plant and herbivore growth and tested the expression of defense-related plant genes to explore potential underlying mechanisms of HIPV mediated seed priming and long-term anti-herbivore defense in future plants.

Results/Conclusions

While the HIPVs cis-3-hexenol and cis-3-hexenyl acetate increased vegetative growth in M. truncatula plants when exposed as seeds, indole generated the strongest and most consistent effect of HIPV seed exposure. Seed exposure to indole reduced the relative growth rate of chewing S. exigua by 30% on A. thaliana plants, and also reduced the weight gain and fecundity of phloem-feeding A. pisum on M. truncatula plants by 28% and 41% respectively. We tested the expression of defense-related genes in indole exposed seed plants with and without herbivory. As expected, herbivory induced the expression of defense marker genes, but gene expressions were not further induced by seed exposure to indole. This suggests indole-mediated seed priming operates through a mechanism autonomous of inducible plant resistance. Ultimately, seed exposure to indole enhanced resistance in two different plant species against different feeding guilds of herbivores, further suggesting a conserved role of indole in mediating plant-seed communication.