Plant seeds are primed by herbivore-induced plant volatiles

Abstract

23Mature plants can detect and respond to herbivore-induced plant volatiles (HIPVs) by priming or 24 directly activating defenses against future herbivores. Whether other plant life stages can respond 25 to HIPVs in similar manners is poorly understood. For example, seeds are known to respond to a 26 variety of environment cues that are essential for proper germination timing and survival. Seeds 27 may also be exposed to HIPVs prior to germination, and such exposure may affect the growth, 28 development, and defense profiles when the seeds grow into mature plants. Here, we investigated 29 the effect of seed exposure to common HIPVs on growth, reproduction and defense 30 characteristics in the model plants Arabidopsis thaliana and Medicago truncatula. Of all the 31 HIPVs tested, indole specifically reduced both beet armyworm growth on A. thaliana and pea 32 aphid fecundity on M. truncatula. Induction of defense genes was not affected by seed exposure 33to indole in either plant species, suggesting that seed priming operates independently of induced 34 resistance. Moreover, neither species showed any negative effect of seed exposure to HIPVs on 35 vegetative and reproductive growth. Rather, M. truncatula plants derived from seeds exposed to 36 z-3-hexanol and z-3-hexenyl acetate grew faster and produced larger leaves compared to 37 controls. Our results indicate that seeds are sensitive to specific HIPVs, which represents a novel 38 ecological mechanism of plant-to-plant communication. 39 40 42 43 44 71 plants against spider mite, caterpillars, aphids, and pathogens (Worrall et al., 2012). Seed 72 treatment with JA also changes the volatile composition of mature plants, making their blends 73 more attractive to predatory mites (Smart et al., 2013). Similarly, seed treatment with salicylic 74 acid (SA) enhances the expression of SA-related genes and the endogenous SA level against root 75 4 holoparasite (Orobanche cumana) (Yang et al., 2016). Additionally, seed coating with plant 76 growth promoting rhizobacteria (PGPR) and plant growth promoting fungus (PGPF) enhances 77 seed germination, seedling establishment, and boosts induced defenses in future plants in 78 ET-, and JA-dependent manners (Ryu et al., 2004; Rudrappa et al., 2010; Sharifi & Ryu, 2016). 79 Seeds also come in contact with biotic agents that are volatile. Inhibitory and allelopathic 80 effects of some plant and microbial derived volatile organic compounds (VOCs) have been . Whereas these VOCs do not 83 necessarily provide contextual information about future environmental conditions, herbivore-84 induced plant volatiles (HIPVs) represent potentially reliable and adaptive indicators of 85 herbivory. The function of HIPVs in priming or directly inducing plant defenses is now well 86 established ( Engelberth et al., 2004; Frost et al., 2007; Rodriguez-Saona & Frost, 2010), and 87 exposure of undamaged plants to HIPVs is known to induce or prime the genes in phytohormone 88 pathways (Bate & Rothstein, 1998; Engelberth et al., 2007; Frost et al.,...

Indole primes defence signalling and increases herbivore resistance in tea plants

“…Indole can also interact with ( Z )‐3‐hexenyl acetate to produce stronger and more specific defence responses and herbivore resistance (Hu et al, 2019). Recent work found that exposure of Arabidopsis thaliana and Medicago truncatula seeds to indole reduces subsequent herbivore performance, suggesting that indole may also promote herbivore resistance in dicotyledonous plants (Maurya, Pazouki, & Frost, 2019). While it has been reported that herbivore attack elicits indole emission in poplar, tea and apple ( Malus × domestica ) plants (Cai, Sun, Dong, Wang, & Chen, 2013; Frost et al, 2007; Giacomuzzi et al, 2016), whether indole can also increase herbivore resistance in woody plants is currently unknown.…”

Sensing the Danger Signals: cis-Jasmone Reduces Aphid Performance on Potato and Modulates the Magnitude of Released Volatiles

“…Similarly, using M. euphoribae, significant lower numbers of newborn nymphs and lower number of settled individuals, with lower weight, were recorded on tomato plants when primed by β-ocimene (Cascone et al, 2015). More recently, Maurya et al (2019) reported a reduced fecundity of pea aphid on barrel medic plants upon their exposure to indole.…”

Integration of multiple volatile cues into plant defense responses

“…Indole is a derivative of the shikimate acid pathway. Exposure to indole primes plant defenses against herbivores in both monocotyledonous and dicotyledonous plants (Maurya et al ., 2019; Ye et al ., 2019). Terpenes are the largest and most structurally diverse class of volatiles.…”