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

PLoS One. 2019 Oct 24;14(10):e0223686. doi: 10.1371/journal.pone.0223686. eCollection 2019.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Division / genetics
  • Computational Biology / methods
  • Gene Expression Profiling*
  • Gene Expression Regulation, Plant
  • Gene Ontology
  • Host-Parasite Interactions / genetics*
  • Host-Pathogen Interactions / genetics*
  • Phenotype
  • Plant Tumors / genetics*
  • Reactive Oxygen Species
  • Signal Transduction
  • Species Specificity
  • Transcriptome*

Substances

  • Reactive Oxygen Species

Grants and funding

This work was supported by JSPS KAKENHI Grant Number 17H06260 and the strategic prioritized research in KPU to IO, ST and MHS, JSPS KAKENHI 16H05068 to MHS, JSPS KAKENHI 18K6366 to ST, JSPS KAKENHI 16H01472, 16K07408, 18H04787, and 18H04844 to SK, and MEXT Supported Program for the Strategic Research Foundation at Private Universities (Grant Number S1511023) to SK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.