Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.

Galls are plant structures generated by gall-inducing organisms including insects, nematodes, fungi, bacteria and viruses. Those made by insects generally consist of inner callus-like cells surrounded by lignified hard cells, supplying both nutrients and protection to the gall insects living inside....

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Main Authors: Seiji Takeda, Makiko Yoza, Taisuke Amano, Issei Ohshima, Tomoko Hirano, Masa H Sato, Tomoaki Sakamoto, Seisuke Kimura
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0223686
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spelling doaj-398d3830a8b649a1abb91b4c22c783bb2021-03-03T21:11:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011410e022368610.1371/journal.pone.0223686Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.Seiji TakedaMakiko YozaTaisuke AmanoIssei OhshimaTomoko HiranoMasa H SatoTomoaki SakamotoSeisuke KimuraGalls are plant structures generated by gall-inducing organisms including insects, nematodes, fungi, bacteria and viruses. Those made by insects generally consist of inner callus-like cells surrounded by lignified hard cells, supplying both nutrients and protection to the gall insects living inside. This indicates that gall insects hijack developmental processes in host plants to generate tissues for their own use. Although galls are morphologically diverse, the molecular mechanism for their development remains poorly understood. To identify genes involved in gall development, we performed RNA-sequencing based transcriptome analysis for leaf galls. We examined the young and mature galls of Glochidion obovatum (Phyllanthaceae), induced by the micromoth Caloptilia cecidophora (Lepidoptera: Gracillariidae), the leaf gall from Eurya japonica (Pentaphylacaceae) induced by Borboryctis euryae (Lepidoptera: Gracillariidae), and the strawberry-shaped leaf gall from Artemisia montana (Asteraceae) induced by gall midge Rhopalomyia yomogicola (Oligotrophini: Cecidomyiidae). Gene ontology (GO) analyses suggested that genes related to developmental processes are up-regulated, whereas ones related to photosynthesis are down-regulated in these three galls. Comparison of transcripts in these three galls together with the gall on leaves of Rhus javanica (Anacardiaceae), induced by the aphid Schlechtendalia chinensis (Hemiptera: Aphidoidea), suggested 38 genes commonly up-regulated in galls from different plant species. GO analysis showed that peptide biosynthesis and metabolism are commonly involved in the four different galls. Our results suggest that gall development involves common processes across gall inducers and plant taxa, providing an initial step towards understanding how they manipulate host plant developmental systems.https://doi.org/10.1371/journal.pone.0223686
collection DOAJ
language English
format Article
sources DOAJ
author Seiji Takeda
Makiko Yoza
Taisuke Amano
Issei Ohshima
Tomoko Hirano
Masa H Sato
Tomoaki Sakamoto
Seisuke Kimura
spellingShingle Seiji Takeda
Makiko Yoza
Taisuke Amano
Issei Ohshima
Tomoko Hirano
Masa H Sato
Tomoaki Sakamoto
Seisuke Kimura
Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
PLoS ONE
author_facet Seiji Takeda
Makiko Yoza
Taisuke Amano
Issei Ohshima
Tomoko Hirano
Masa H Sato
Tomoaki Sakamoto
Seisuke Kimura
author_sort Seiji Takeda
title Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
title_short Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
title_full Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
title_fullStr Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
title_full_unstemmed Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
title_sort comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2019-01-01
description Galls are plant structures generated by gall-inducing organisms including insects, nematodes, fungi, bacteria and viruses. Those made by insects generally consist of inner callus-like cells surrounded by lignified hard cells, supplying both nutrients and protection to the gall insects living inside. This indicates that gall insects hijack developmental processes in host plants to generate tissues for their own use. Although galls are morphologically diverse, the molecular mechanism for their development remains poorly understood. To identify genes involved in gall development, we performed RNA-sequencing based transcriptome analysis for leaf galls. We examined the young and mature galls of Glochidion obovatum (Phyllanthaceae), induced by the micromoth Caloptilia cecidophora (Lepidoptera: Gracillariidae), the leaf gall from Eurya japonica (Pentaphylacaceae) induced by Borboryctis euryae (Lepidoptera: Gracillariidae), and the strawberry-shaped leaf gall from Artemisia montana (Asteraceae) induced by gall midge Rhopalomyia yomogicola (Oligotrophini: Cecidomyiidae). Gene ontology (GO) analyses suggested that genes related to developmental processes are up-regulated, whereas ones related to photosynthesis are down-regulated in these three galls. Comparison of transcripts in these three galls together with the gall on leaves of Rhus javanica (Anacardiaceae), induced by the aphid Schlechtendalia chinensis (Hemiptera: Aphidoidea), suggested 38 genes commonly up-regulated in galls from different plant species. GO analysis showed that peptide biosynthesis and metabolism are commonly involved in the four different galls. Our results suggest that gall development involves common processes across gall inducers and plant taxa, providing an initial step towards understanding how they manipulate host plant developmental systems.
url https://doi.org/10.1371/journal.pone.0223686
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