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      Transcriptome profile of cup-shaped galls in Litsea acuminata leaves

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          Abstract

          Background

          Insect galls are atypical plant tissues induced by the invasion of insects. Compared to the host leaf, gall tissues lose photosynthetic ability, but have higher soluble sugar content. Although the physiological and biochemical regulation of gall tissues have been demonstrated, the mechanism of genetic regulation has only been analyzed in few studies.

          Results

          In this study, the transcriptome of cup-shaped galls and its host leaf were de novo assembled. Cellular functional enrichment and differentially expressed gene groups in the gall tissues were analyzed. The genes associated with primary metabolism, including photosynthesis, cell wall turnover, and sugar degradation, were expressed differently in galls and leaves. The examination of gene expression demonstrated that the genes involved in brassinosteroid synthesis and responses exhibited a remarkable modulation in cup-shaped galls, suggesting a potential role of steroid hormones in regulating gall development.

          Conclusions

          This study revealed the genetic responses, including those involved in source-sink reallocation and phytohormone metabolism, of galls induced by a dipteran insect.

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          Most cited references25

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          Role of phytohormones in insect-specific plant reactions.

          The capacity to perceive and respond is integral to biological immune systems, but to what extent can plants specifically recognize and respond to insects? Recent findings suggest that plants possess surveillance systems that are able to detect general patterns of cellular damage as well as highly specific herbivore-associated cues. The jasmonate (JA) pathway has emerged as the major signaling cassette that integrates information perceived at the plant-insect interface into broad-spectrum defense responses. Specificity can be achieved via JA-independent processes and spatio-temporal changes of JA-modulating hormones, including ethylene (ET), salicylic acid (SA), abscisic acid (ABA), auxin, cytokinins (CK), brassinosteroids (BR) and gibberellins (GB). The identification of receptors and ligands and an integrative view of hormone-mediated response systems are crucial to understand specificity in plant immunity to herbivores. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            Soluble sugars--metabolism, sensing and abiotic stress: a complex network in the life of plants.

            Plants are autotrophic and photosynthetic organisms that both produce and consume sugars. Soluble sugars are highly sensitive to environmental stresses, which act on the supply of carbohydrates from source organs to sink ones. Sucrose and hexoses both play dual functions in gene regulation as exemplified by the upregulation of growth-related genes and downregulation of stress-related genes. Although coordinately regulated by sugars, these growth- and stress-related genes are upregulated or downregulated through HXK-dependent and/or HXK-independent pathways. Sucrose-non-fermenting-1- (SNF1-) related protein pathway, analogue to the protein kinase (SNF-) yeast-signalling pathway, seems also involved in sugar sensing and transduction in plants. However, even if plants share with yeast some elements involved in sugar sensing, several aspects of sugar perception are likely to be peculiar to higher plants. In this paper, we have reviewed recent evidences how plants sense and respond to environmental factors through sugar-sensing mechanisms. However, we think that forward and reverse genetic analysis in combination with expression profiling must be continued to uncover many signalling components, and a full biochemical characterization of the signalling complexes will be required to determine specificity and cross-talk in abiotic stress signalling pathways.
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              Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling.

              Salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and their interactions mediate plant responses to pathogen and herbivore attack. JA-SA and JA-ET cross-signaling are well studied, but little is known about SA-ET cross-signaling in plant-herbivore interactions. When the specialist herbivore tobacco hornworm (Manduca sexta) attacks Nicotiana attenuata, rapid and transient JA and ET bursts are elicited without significantly altering wound-induced SA levels. In contrast, attack from the generalist beet armyworm (Spodoptera exigua) results in comparatively lower JA and ET bursts, but amplified SA bursts. These phytohormone responses are mimicked when the species' larval oral secretions (OS(Se) and OS(Ms)) are added to puncture wounds. Fatty acid-amino acid conjugates elicit the JA and ET bursts, but not the SA burst. OS(Se) had enhanced glucose oxidase activity (but not beta-glucosidase activity), which was sufficient to elicit the SA burst and attenuate the JA and ET levels. It is known that SA antagonizes JA; glucose oxidase activity and associated hydrogen peroxide also antagonizes the ET burst. We examined the OS(Ms)-elicited SA burst in plants impaired in their ability to elicit JA (antisense [as]-lox3) and ET (inverted repeat [ir]-aco) bursts and perceive ET (35s-etr1b) after fatty acid-amino acid conjugate elicitation, which revealed that both ET and JA bursts antagonize the SA burst. Treating wild-type plants with ethephone and 1-methylcyclopropane confirmed these results and demonstrated the central role of the ET burst in suppressing the OS(Ms)-elicited SA burst. By suppressing the SA burst, the ET burst likely facilitates unfettered JA-mediated defense activation in response to herbivores that otherwise would elicit SA.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – original draft
                Role: ConceptualizationRole: Resources
                Role: Formal analysisRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                24 October 2018
                2018
                : 13
                : 10
                : e0205265
                Affiliations
                [1 ] Biodiversity Research Center, Academia Sinica, Nankang, Taipei, Taiwan
                [2 ] Department of Horticulture and Biotechnology, Chinese Culture University, Shihlin, Taipei, Taiwan
                [3 ] Department of Life Science, National Taiwan Normal University, Wenshan, Taipei, Taiwan
                Fred Hutchinson Cancer Research Center, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2287-0667
                Article
                PONE-D-18-04369
                10.1371/journal.pone.0205265
                6200225
                30356295
                08494278-1896-4d44-919b-45e5ee8aedc8
                © 2018 Shih et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 25 February 2018
                : 22 September 2018
                Page count
                Figures: 7, Tables: 2, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: 104-2621-B-001-007
                Award Recipient :
                Our works were supported by the Ministry of Science and Technology, Taiwan (104-2621-B-001- 007).
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Insect Interactions
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Insect Interactions
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Plant-Insect Interactions
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Biochemistry
                Hormones
                Plant Hormones
                Cytokinins
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Plant Hormones
                Cytokinins
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Plant Hormones
                Cytokinins
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Physiology
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Invertebrate Physiology
                Insect Physiology
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                All relevant data are within the paper and its Supporting Information files.

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