Honeydew-associated microbes elicit defense responses against brown planthopper in rice

Feeding of sucking insects, such as the rice brown planthopper (Nilaparvata lugens; BPH), causes only limited mechanical damage on plants that is otherwise essential for injury-triggered defense responses against herbivores. In pursuit of complementary BPH elicitors perceived by plants, we examined the potential effects of BPH honeydew secretions on the BPH monocot host, rice (Oryza sativa). We found that BPH honeydew strongly elicits direct and putative indirect defenses in rice, namely accumulation of phytoalexins in the leaves, and release of volatile organic compounds from the leaves that serve to attract natural enemies of herbivores, respectively. We then examined the elicitor active components in the honeydew and found that bacteria in the secretions are responsible for the activation of plant defense. Corroborating the importance of honeydew-associated microbiota for induced plant resistance, BPHs partially devoid of their microbiota via prolonged antibiotics ingestion induced significantly less defense in rice relative to antibiotic-free insects applied to similar groups of plants. Our data suggest that rice plants may additionally perceive herbivores via their honeydew-associated microbes, allowing them to discriminate between incompatible herbivores—that do not produce honeydew—and those that are compatible and therefore dangerous

Herbivore-induced and constitutive volatiles are controlled by different oxylipin-dependent mechanisms in rice

Despite the importance of volatile organic compounds (VOCs) for plants, control mechanisms for their basal and stress-induced biosynthesis and release remain unclear. We sampled and characterized headspace and internal leaf volatile pools in rice (Oryza sativa), after a simulated herbivory treatment, which triggers an endogenous jasmonate burst. Certain volatiles, such as linalool, were strongly upregulated by simulated herbivory stress. In contrast, other volatiles, such as β-caryophyllene, were constitutively emitted and fluctuated according to time of day. Transcripts of the linalool synthase gene transiently increased 1–3 h after exposure of rice to simulated herbivory, whereas transcripts of caryophyllene synthase peaked independently at dawn. Unexpectedly, although emission and accumulation patterns of rice inducible and constitutive VOCs were substantially different, both groups of volatiles were compromised in jasmonate-deficient hebiba mutants, which lack the allene oxide cyclase (AOC) gene. This suggests that rice employs at least two distinct oxylipin-dependent mechanisms downstream of AOC to control production of constitutive and herbivore-induced volatiles. Levels of the JA precursor, 12-oxo-phytodienoic acid (OPDA), were correlated with constitutive volatile levels suggesting that OPDA or its derivatives could be involved in control of volatile emission in rice

Comparative analysis of sorghum (C4) and rice (C3) plant headspace volatiles induced by artificial herbivory

Acute stress responses include release of defensive volatiles from herbivore-attacked plants. Here we used two closely related monocot species, rice as a representative C3 plant, and sorghum as a representative C4 plant, and compared their basal and stress-induced headspace volatile organic compounds (VOCs). Although both plants emitted similar types of constitutive and induced VOCs, in agreement with the close phylogenetic relationship of the species, several mono- and sesquiterpenes have been significantly less abundant in headspace of sorghum relative to rice. Furthermore, in spite of generally lower VOC levels, some compounds, such as the green leaf volatile (Z)-3-hexenyl acetate and homoterpene DMNT, remained relatively high in the sorghum headspace, suggesting that a separate mechanism for dispersal of these compounds may have evolved in this plant. Finally, a variable amount of several VOCs among three sorghum cultivars of different geographical origins suggested that release of VOCs could be used as a valuable resource for the increase of sorghum resistance against herbivores

The diurnal emission pattern of constitutive and induced rice volatiles

Plants have evolved highly effective defense mechanisms to resist attacks by herbivores. Insect resistance traits include 'indirect defense' which is the ability to respond to herbivore attack by synthesizing a complex bouquet of herbivore-induced volatile organic compounds (HI-VOCs) that attract natural enemies of herbivores. Using the trophic model of rice plant and the generalist Loreyi armyworm, Mythimna loreyi Duponchel (MYL), we characterized the inducibility of rice HI-VOCs upon MYL mimicked herbivory. Our results show that simulated MYL feeding significantly increases the emission of a number of key HI-VOCs, including linalool and MeSA. Given that many abiotic factors affect VOCs emissions, such as the photoperiod (Gouinguené and Turlings 2002), the diurnal emission patterns of HI-VOCs were determined in control rice plants and those subjected to MYL simulated feeding on a previous day. Our findings stress that both control and induced rice plants followed a diurnal pattern in VOCs emission; however, induced plants emitted remarkably higher amounts of HI-VOCs, 2-10 folds in some compounds, compared with control plants. It suggests that such enhanced HI-VOCs blend and its composition fully depends on the photoperiod of the environment when the natural enemies are actively foraging during the day.status: publishe

Profiling of volatile organic compound (VOC) emissions in rice plants

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Characterization of herbivore-induced rice volatiles under real and mimic herbivory

Herbivores and carnivores use plant volatiles as information for effective foraging. To elucidate the impact of herbivory or mechanical wounding on VOCs profile in rice, we challenged the rice plants by either real herbivory of the generalist herbivore Mythimna loreyi Duponchel (MYL) or mimic infestation by mechanical damage with application of MYL regurgitant, whereas plants were only wounded for the mechanical damage treatment. Overall, real or mimic herbivory notably induced the emission of VOCs compared to wounded or control plants. In our current experimental set-up, green leave volatiles (GLVs) were induced by mimic herbivory or wounding, but not with real MYL feeding. Aromatic compounds as indole showed significant induction by real or mimic herbivory as well as wounding. No significant induction was reported for constitutive terpenoids such as limonene, however some sesquiterpenes showed slight, significant in some compounds, induction under both herbivory treatments.status: publishe

The diurnal emission pattern of constitutive and induced rice volatiles

Plants have evolved highly effective defense mechanisms to resist attacks by herbivores. Insect resistance traits include 'indirect defense' which is the ability to respond to herbivore attack by synthesizing a complex bouquet of herbivore-induced volatile organic compounds (HI-VOCs) that attract natural enemies of herbivores. Using the trophic model of rice plant and the generalist Loreyi armyworm, Mythimna loreyi Duponchel (MYL), we characterized the inducibility of rice HI-VOCs upon MYL mimicked herbivory. Our results show that simulated MYL feeding significantly increases the emission of a number of key HI-VOCs, including linalool and MeSA. Given that many abiotic factors affect VOCs emissions, such as the photoperiod (Gouinguené and Turlings 2002), the diurnal emission patterns of HI-VOCs were determined in control rice plants and those subjected to MYL simulated feeding on a previous day. Our findings stress that both control and induced rice plants followed a diurnal pattern in VOCs emission; however, induced plants emitted remarkably higher amounts of HI-VOCs, 2-10 folds in some compounds, compared with control plants. It suggests that such enhanced HI-VOCs blend and its composition fully depends on the photoperiod of the environment when the natural enemies are actively foraging during the day

Oral Secretions Affect HIPVs Induced by Generalist (Mythimna loreyi) and Specialist (Parnara guttata) Herbivores in Rice

Plants synthesize variable mixtures of herbivore induced plant volatiles (HIPVs) as part of their evolutionary conserved defense. To elucidate the impact of chewing herbivores with different level of adaptation on HIPV profiles in rice, we measured HIPVs released from rice seedlings challenged by either the generalist herbivore Mythimna loreyi (MYL) or the specialist Parnara guttata (PAG). Both herbivores markedly elicited the emission of HIPVs, mainly on the second and third days after attack compared to control plants. In addition, side-by-side HIPV comparisons using MYL and PAG caterpillars revealed that generalist feeding induced comparably more HIPVs relative to specialist, particularly on day two as highlighted by multivariate analysis (PLS-DA) of emitted HIPVs, and further confirmed in mimicked herbivory experiments. Here, mechanically wounded plants treated with water (WW) released more VOCs than untreated controls,and on top of this, oral secretions (OS) from both herbivores showed differential effects on volatile emissions from the wounded plants. Similar to actual herbivory, MYL OS promoted higher amounts of HIPVs relative to PAG OS, thus supporting disparate induction of rice indirect defenses in response to generalist and specialist herbivores, which could be due to the differential composition of their OS.status: publishe