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

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.

SUBMITTER: Wari D

PROVIDER: S-EPMC6411376 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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

Wari David D Kabir Md Alamgir MA Mujiono Kadis K Hojo Yuko Y Shinya Tomonori T Tani Akio A Nakatani Hiroko H Galis Ivan I

Journal of experimental botany 20190301 5

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 accumul ...[more]

PMID: 30715410

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Project description:BACKGROUND:Host adaptation is the primary determinant of insect diversification. However, knowledge of different host ranges in closely related species remains scarce. The brown planthopper (Nilaparvata lugens, BPH) and the small brown planthopper (Laodelphax striatellus, SBPH) are the most destructive insect pests within the family Delphacidae. These two species differ in their host range (SBPH can well colonize rice and wheat plants, whereas BPH survives on only rice plants), but the underlying mechanism of this difference remains unknown. High-throughput sequencing provides a powerful approach for analyzing the association between changes in gene expression and the physiological responses of insects. Therefore, gut transcriptomes were performed to elucidate the genes associated with host adaptation in planthoppers. The comparative analysis of planthopper responses to different diets will improve our knowledge of host adaptation regarding herbivorous insects. RESULTS:In the present study, we analyzed the change in gene expression of SBPHs that were transferred from rice plants to wheat plants over the short term (rSBPH vs tSBPH) or were colonized on wheat plants over the long term (rSBPH vs wSBPH). The results showed that the majority of differentially expressed genes in SBPH showed similar changes in expression for short-term transfer and long-term colonization. Based on a comparative analysis of BPH and SBPH after transfer, the genes associated with sugar transporters and heat-shock proteins showed similar variation. However, most of the genes were differentially regulated between the two species. The detoxification-related genes were upregulated in SBPH after transfer from the rice plants to the wheat plants, but these genes were downregulated in BPH under the same conditions. In contrast, ribosomal-related genes were downregulated in SBPH after transfer, but these genes were upregulated in BPH under the same conditions. CONCLUSIONS:The results of this study provide evidence that host plants played a dominant role in shaping gene expression and that the low fitness of BPH on wheat plants might be determined within 24?h after transfer. This study deepens our understanding of different host ranges for the two planthopper species, which may provide a potential strategy for pest management.

Dataset Information

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

Publications

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

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