Abstract
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.
Highlights
The rice brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is one of the most serious pests of rice in Asia
To confirm that these phytoalexins are induced in intact plants, the last fully developed leaves of the 6-week-old rice seedlings were treated with 2 μl of crude honeydew, which was gently rubbed on the leaf surface.While metabolite induction was not observed at 24 h and 48 h post-treatment, FP and another herbivoryinduced leaf phytoalexin, feruloylagmatine (FA), accumulated more at 72 h post-treatment compared to control leaves (Fig 2; Supplementary Fig. S2)
We show that microbes from honeydew of BPHs can effectively elicit rice defenses.The antibiotics fed to BPHs suppressed cultivable microbes in the honeydew, which in turn attenuated the inducible defenses of rice against BPHs.We propose a model in which microbes in honeydew are perceived by rice to amplify its defense, which acts in addition to elicitors found in the BPH salivary secretions, and mechanical damage of various sources
Summary
The rice brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is one of the most serious pests of rice in Asia. It is alarming that a sharp increase in the frequency and extent of hopper outbreaks has been noticed since ~2002, resulting in gross losses of rice crop, in China, Thailand, and Vietnam (Fujita et al, 2013). Rice damage (often called ‘hopper burn’ as opposed to viral symptoms) results from extensive feeding of hoppers, and extraction of phloem sap by means of a stylet protected by a salivary sheath (Wang et al, 2008).
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