Reprogramming of the Developmental Program of Rhus javanica During Initial Stage of Gall Induction by Schlechtendalia chinensis.

Tomoko Hirano,Seisuke Kimura,Tomoaki Sakamoto,Issei Ohshima,Takakazu Matsuura,Yoko Ikeda,Takumi Nakayama,Masa H Sato,Ayaka Okamoto,Seiji Takeda,Yoshihito Suzuki

doi:10.3389/fpls.2020.00471

Abstract

Insect galls are unique organs that provide shelter and nutrients to the gall-inducing insects. Although insect galls are fascinating structures for their unique shapes and functions, the process by which gall-inducing insects induce such complex structures is not well understood. Here, we performed RNA-sequencing-based comparative transcriptomic analysis of the early developmental stage of horned gall to elucidate the early gall-inducing process carried out by the aphid, Schlechtendalia chinensis, in the Chinese sumac, Rhus javanica. There was no clear similarity in the global gene expression profiles between the gall tissue and other tissues, and the expression profiles of various biological categories such as phytohormone metabolism and signaling, stress-response pathways, secondary metabolic pathways, photosynthetic reaction, and floral organ development were dramatically altered. Particularly, master transcription factors that regulate meristem, flower, and fruit development, and biotic and abiotic stress-responsive genes were highly upregulated, whereas the expression of genes related to photosynthesis strongly decreased in the early stage of the gall development. In addition, we found that the expression of class-1 KNOX genes, whose ectopic overexpression is known to lead to the formation of de novo meristematic structures in leaf, was increased in the early development stage of gall tissue. These results strengthen the hypothesis that gall-inducing insects convert source tissues into fruit-like sink tissues by regulating the gene expression of host plants and demonstrate that such manipulation begins from the initial process of gall induction.

Highlights

Galls are plant tissues or organs formed by hyperplasia and/or hypertrophy induced by parasitic or pathogenic organisms including viruses, fungi, bacteria, nematodes, mites, and insects (Mani, 1964)
Liu et al (2014) reported the histological analysis of the developmental process of R. chinensis gall; they categorized the developmental process of the gall into six different phases
We revealed that the photosynthesisrelated genes involved in the photosystem I (GO: 0009768), photosystem II (GO: 0009769), and carbon fixation pathway (GO: 0015977) were dramatically downregulated during the early gall development in R. chinensis

Summary

INTRODUCTION

Galls are plant tissues or organs formed by hyperplasia (increased cell number) and/or hypertrophy (increased cell size) induced by parasitic or pathogenic organisms including viruses, fungi, bacteria, nematodes, mites, and insects (Mani, 1964). Drastic morphological rearrangement occurs in the leaf wing tissues, in which the palisade tissues of the galled leaf wings are reorganized and replaced by parenchyma cells, and galled zones connect to nongalled zones by newly formed vascular bundles (Liu et al, 2014) Such complexity both in the developmental process and in the structure of S. chinensis galls implies that modified but well-organized host-plant gene networks could be incorporated in the process of gall development. The genes involved in the phytohormone metabolic and signaling pathways, abiotic and biotic stress responses, and organ development were significantly upregulated, whereas photosynthetic genes were dramatically downregulated These results imply that the gall-inducing aphid manipulates the plant reproductive programs to convert source tissues into fruit-like sink tissues during the initial process of gall induction

MATERIALS AND METHODS

RESULTS

DATA AVAILABILITY STATEMENT