Duplication and expression of horizontally transferred polygalacturonase genes is associated with host range expansion of mirid bugs

Jiangtao Chao,Robert Holdbrook,Bin Lu,Yanhui Lu,Jinyan Liu,Philip Donkersley,Pengjun Xu

doi:10.1186/s12862-019-1351-1

Abstract

BackgroudHorizontal gene transfer and gene duplication are two major mechanisms contributing to the evolutionary adaptation of organisms. Previously, polygalacturonase genes (PGs) were independently horizontally transferred and underwent multiple duplications in insects (e.g., mirid bugs and beetles). Here, we chose three phytozoophagous mirid bugs (Adelphocoris suturalis, A. fasciaticollis, A. lineolatus) and one zoophytophagous mirid bug (Nesidiocoris tenuis) to detect whether the duplication, molecular evolution, and expression levels of PGs were related to host range expansion in mirid bugs.ResultsBy RNA-seq, we reported 30, 20, 19 and 8 PGs in A. suturalis, A. fasciaticollis, A. lineolatus and N. tenuis, respectively. Interestingly, the number of PGs was significantly positive correlation to the number of host plants (P = 0.0339) in mirid bugs. Most PGs (> 17) were highly expressed in the three phytozoophagous mirid bugs, while only one PG was relatively highly expressed in the zoophytophagous mirid bug. Natural selection analysis clearly showed that a significant relaxation of selection pressure acted on the PGs in zoophytophagous mirid bugs (K = 0.546, P = 0.0158) rather than in phytozoophagous mirid bugs (K = 1, P = 0.92), suggesting a function constraint of PGs in phytozoophagous mirid bugs.ConclusionTaken together with gene duplication, molecular evolution, and expression levels, our results suggest that PGs are more strictly required by phytozoophagous than by zoophytophagous mirid bugs and that the duplication of PGs is associated with the expansion of host plant ranges in mirid bugs.

Highlights

Horizontal gene transfer (HGT) and gene duplication are two major mechanisms contributing to the evolutionary adaptation of organisms [1,2,3,4,5,6]
The RNA-seq data were submitted to the National Center for Biotechnology Information (NCBI) Gene Expression Omnibus (GEO) database [40], and Sequence Read Archive (SRA) database
With functional annotation and a BLAST search using 202 polygalacturonase genes (PGs) as reference sequences, we found 30, 20, 19, and 7 PGs in A. suturalis, A. fasciaticollis, A. lineolatus, and N. tenuis, respectively (Additional file 1: Table S3-S6)

Summary

Introduction

Horizontal gene transfer (HGT) and gene duplication are two major mechanisms contributing to the evolutionary adaptation of organisms [1,2,3,4,5,6]. PGs have been detected in some insects from Hemiptera and Coleoptera, such as mirid bugs and leaf beetles [14,15,16]. The genes encoding PG proteins were cloned from mirid bugs and leaf beetles, and phylogenetic analysis suggested these genes were horizontally transferred to mirids from fungi and had undergone multiple duplications [14, 16, 21]. The duplication of digestive enzymes (PG genes) was considered as potentially expanding the host plant range of these insects [14, 15]

Methods

Results

Discussion

Conclusion