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Front Plant Sci
2018 Jan 01;9:1521. doi: 10.3389/fpls.2018.01521.
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Structural and Chemical Profiles of Myrcia splendens (Myrtaceae) Leaves Under the Influence of the Galling Nexothrips sp. (Thysanoptera).
Jorge NC
,
Souza-Silva ÉA
,
Alvarenga DR
,
Saboia G
,
Soares GLG
,
Zini CA
,
Cavalleri A
,
Isaias RMS
.
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Thysanoptera-induced galls commonly culminate in simple folding or rolling leaf gall morphotypes. Most of these galls are induced by members of the suborder Tubulifera, with only a few species of the suborder Terebrantia being reported as gall inducers. The Terebrantia, as most of the gall inducers, manipulates the host plant cellular communication system, and induces anatomical and biochemical changes in its host plant. In an effort to keep its homeostasis, the host plant reacts to the stimuli of the galling insect and triggers chemical signaling processes. In contrast to free-living herbivores, the signaling processes involving galling herbivores and their host plants are practically unknown. Current investigation was performed into two steps: first, we set the structural profile of non-galled and galled leaves, and looked forward to find potential alterations due to gall induction by an undescribed species of Nexothrips (suborder Terebrantia) on Myrcia splendens. Once oil glands had been altered in size and number, the second step was the investigation of the chemical profile of three tissue samples: (1) non-galled leaves of a control individual, (2) non-galled leaves of galled plants, and (3) galls. This third sample was divided into two groups: (3.1) galls from which the inducing thrips were manually removed and (3.2) galls macerated with the inducing thrips inside. The chemical profile was performed by gas chromatography/ mass spectrometric detector after headspace solid-phase extraction. The galling activity of the Nexothrips sp. on M. splendens culminates in mesophyll compactness interspersed to diminutive hypersensitive spots, development of air cavities, and the increase in size and number of the secretory glands. Seventy-two compounds were completely identified in the volatile profile of the three samples, from which, sesquiterpenes and aldehydes, pertaining to the "green leaf volatile" (GLVs) class, are the most abundant. The rare event of gall induction by a Terebrantia revealed discrete alterations toward leaf rolling, and indicated quantitative differences related to the plant bioactivity manipulated by the galling thrips. Also, the content of methyl salicylate has varied and has been considered a potential biomarker of plant resistance stimulated as a long-distance effect on M.splendens individuals.
FIGURE 1. Non-galled leaves and galls induced on leaves of Myrcia splendens by an undescribed species of Nexothrips (suborder Terebrantia) (A) Non-galled leaves and stem branch with leaf rolling galls. (B) Anatomy of non-galled leaves, evidencing the mesophyll and oil glands. (C) Gall mesophyll, evidencing the hypersensitive reaction in response to the inducer’s feeding activity. (D) Anatomy of a gall, evidencing the increased number of secretory cavities. (E) Gall mesophyll, evidencing the reduction of intercellular spaces and air cavities. Arrowhead: Non-galled leaves, Dashed: Rolling gall, OG: Oil gland, OV: Oviposition, HR: Hypersensitive area, Arrow: Air cavities Scale bars: A: 2 cm, B,C,E: 50 μm; D: 200 μm.
FIGURE 2. Oviposition inside the tissues of a M. splendens rolling gall induced by an undescribed species of Nexothrips (suborder Terebrantia). (A) Initial development of the larva inside gall tissues. (B) Development of the larva. (C,D) Larvae hatching out of gall tissues. (C) Anatomy of a gall, evidencing hatching out of the leaf tissue. (D) MEV slides evidencing the hatching. L: Larva, OV: oviposition, HR: Hypersensitive area. Scale bars: A–C: 50 μm; D: 10 μm.
FIGURE 3. Quantitative analysis of glands. (A) Density of the glands per mm2. (B) Glands area. NGL: Non-galled leaves.
FIGURE 4. Profile of the distribution of VOCs in non-galled leaves and galls. Plot depicts the distribution of VOC profiles of leaves (non-galled samples, including NGL and Ctrl) and galls (including LRGwT and cLRG samples) over the PCA score plot defined by the first two principal components.
FIGURE 5. Profile of the distribution of VOCs in non-galled leaves and galls. Plot shows the heat map distribution of the 25 most discriminating VOCs identified by SPME-GC-MS analysis. Color key indicates metabolite expression value, blue: Lowest, red: highest.
FIGURE 6. Box plots of top metabolites that significantly differed between leaves and galls. (A) VOCs up regulated in gall samples. (B) VOCs down regulated in gall samples.
FIGURE 7. Heat map of non-galled leaves. The heat maps were constructed based on the 25 most discriminating compounds. Compounds identified by HS-SPME-GC/MS. Color key indicates metabolite expression value, blue: Lowest, red: highest.
FIGURE 8. Heat map of galls. The heat maps were constructed based on the 25 most discriminating compounds. Compounds identified by HS-SPME-GC/MS. Color key indicates metabolite expression value, blue: Lowest, red: highest.
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