RESUMEN
Plants perceive herbivory-induced volatiles and respond to them by upregulating their defenses. To date, the organs responsible for volatile perception remain poorly described. Here, we show that responsiveness to the herbivory-induced green leaf volatile (Z)-3-hexenyl acetate (HAC) in terms of volatile emission, transcriptional regulation, and jasmonate defense hormone activation is largely constrained to younger maize leaves. Older leaves are much less sensitive to HAC. In a given leaf, responsiveness to HAC is high at immature developmental stages and drops off rapidly during maturation. Responsiveness to the non-volatile elicitor ZmPep3 shows an opposite pattern, demonstrating that this form of hyposmia (i.e., decreased sense of smell) is not due to a general defect in jasmonate defense signaling in mature leaves. Neither stomatal conductance nor leaf cuticle composition explains the unresponsiveness of older leaves to HAC, suggesting perception mechanisms upstream of jasmonate signaling as driving factors. Finally, we show that hyposmia in older leaves is not restricted to HAC and extends to the full blend of herbivory-induced volatiles. In conclusion, our work identifies immature maize leaves as dominant stress volatile-sensing organs. The tight spatiotemporal control of volatile perception may facilitate within plant defense signaling to protect young leaves and may allow plants with complex architectures to explore the dynamic odor landscapes at the outer periphery of their shoots.
Asunto(s)
Anosmia , Zea mays , Zea mays/genética , Ciclopentanos , HerbivoriaRESUMEN
Several herbivorous caterpillars contain effectors in their oral secretions that alter the emission of green leaf volatiles (GLVs) produced by the plants upon which the caterpillars are feeding. These effectors include an isomerase, a fatty acid dehydratase (FHD), and a heat-stable hexenal trapping (HALT) molecule. GLVs serve as signaling compounds in plant-insect interactions and inter-and intra-plant communication. However, it is not known whether these GLV-altering effectors are common among herbivorous caterpillars, or the evolutionary context of these effectors in relation to GLV emission by host plants in response to feeding damage. Here, we examined the distribution and activity of the isomerase, FHD, and HALT effectors across 10 species spanning 7 lepidopteran families. Six of the 10 species possessed all three effectors in their oral secretions. Activity from the HALT and FHD effectors was observed in all examined caterpillar species, while activity from the isomerase effector varied in some species and was absent in others. There was no discernable pattern in effector activity based on evolutionary divergence, since individual species within a family did not possess similar mechanisms to alter GLV emission. These data, demonstrating the GLV-altering effectors acting at different steps in the GLV biosynthetic pathway and present in the examined caterpillar species at different combinations with different activities, highlight the importance of these effectors in changing the emission of these compounds during caterpillar herbivory. Understanding the prevalence and roles of GLV-altering effectors and GLV emission itself will open new research areas in the dynamics of plant-insect interactions.
Asunto(s)
Herbivoria , Compuestos Orgánicos Volátiles , Animales , Herbivoria/fisiología , Humanos , Insectos/metabolismo , Larva/fisiología , Hojas de la Planta/metabolismo , Compuestos Orgánicos Volátiles/metabolismoRESUMEN
Evidence that plants can respond to volatile organic compounds (VOCs) was first presented 35 years ago. Since then, over 40 VOCs have been found to induce plant responses. These include VOCs that are produced not only by plants but also by microbes and insects. Here, we summarize what is known about how these VOCs are produced and how plants detect and respond to them. In doing so, we highlight notable observations we believe are worth greater consideration. For example, the VOCs that induce plant responses appear to have little in common. They are derived from many different biosynthetic pathways and have few distinguishing chemical or structural features. Likewise, plants appear to use several mechanisms to detect VOCs rather than a single dedicated "olfactory" system. Considering these observations, we advocate for more discovery-oriented experiments and propose that future research take a fresh look at the ways plants detect and respond to VOCs.
Asunto(s)
Fitoquímicos/química , Fenómenos Fisiológicos de las Plantas , Plantas/química , Compuestos Orgánicos Volátiles/química , Reguladores del Crecimiento de las Plantas/química , Terpenos/químicaRESUMEN
Although considerable evidence has accumulated on the defensive activity of plant volatile organic compounds against pathogens and insect herbivores, less is known about the significance of volatile organic compounds emitted by plants under abiotic stress. Here, we report that green leaf volatiles (GLVs), which were previously shown to prime plant defences against insect herbivore attack, also protect plants against cold stress (4 °C). We show that the expression levels of several cold stress-related genes are significantly up-regulated in maize (Zea mays) seedlings treated with physiological concentrations of the GLV, (Z)-3-hexen-1-yl acetate (Z-3-HAC), and that seedlings primed with Z-3-HAC exhibit increased growth and reduced damage after cold stress relative to unprimed seedlings. Together, these data demonstrate the protective and priming effect of GLVs against cold stress and suggest an activity of GLVs beyond the activation of typical plant defence responses against herbivores and pathogens.
Asunto(s)
Hojas de la Planta/metabolismo , Compuestos Orgánicos Volátiles/metabolismo , Zea mays/metabolismo , Respuesta al Choque por Frío , Expresión Génica , Hojas de la Planta/fisiología , Plantones/metabolismo , Plantones/fisiología , Zea mays/fisiologíaRESUMEN
Previously, we described a priming effect of α-linolenic acid (LnA) on anti-herbivore defense response in maize seedlings. 1 We showed that exogenous application of LnA stimulated higher jasmonic acid (JA) accumulation and herbivore-induced plant volatile (HIPV) emission after treatment with insect elicitor (IE). To further investigate the specificity of LnA's priming effect, we incubated maize seedlings in palmitoleic acid (PeicA), γ-linolenic acid (γ LnA) and stearic acid (StA) solutions, and analyzed HIPV emission in response to IE. Seedlings incubated in PeicA and γ LnA had 3 and 1.8 times higher HIPV release when compared to controls. In contrast, treatment with StA did not up-regulate HIPV release. We propose that the elevated level and/or the presence of unsaturated fatty acids sensitize the defense signaling system, which in turn augments the defense response of maize when under insect herbivore attack.