Proto-oncogenes in a eukaryotic unicellular organism play essential roles in plasmodial growth in host cells

Kai Bi,Tao Chen,Yanping Fu,Jiatao Xie,Jiasen Cheng,Daohong Jiang,Zhixiao Gao,Ying Zhao,Zhangchao He

doi:10.1186/s12864-018-5307-4

Abstract

BackgroundThe eukaryotic unicellular protist Plasmodiophora brassicae is an endocellular parasite of cruciferous plants. In host cortical cells, this protist develops a unicellular structure that is termed the plasmodium. The plasmodium is actually a multinucleated cell, which subsequently splits and forms resting spores. The mechanism for the growth of this endocellular parasite in host cell is unclear.ResultsHere, combining de novo genome sequence and transcriptome analysis of strain ZJ-1, we identified top five significant enriched KEGG pathways of differentially expressed genes (DEGs), namely translation, cell growth and death, cell communication, cell motility and cancers. We detected 171 proto-oncogenes from the genome of P. brassicae that were implicated in cancer-related pathways, of which 46 were differential expression genes. Three predicted proto-oncogenes (Pb-Raf1, Pb-Raf2, and Pb-MYB), which showed homology to the human proto-oncogenes Raf and MYB, were specifically activated during the plasmodial growth in host cortical cells, demonstrating their involvement in the multinucleate development stage of the unicellular protist organism. Gene networks involved in the tumorigenic-related signaling transduction pathways and the activation of 12 core genes were identified. Inhibition of phosphoinositol-3-kinase relieved the clubroot symptom and significantly suppressed the development process of plasmodia.ConclusionsProto-oncogene-related regulatory mechanisms play an important role in the plasmodial growth of P. brassicae.

Highlights

The eukaryotic unicellular protist Plasmodiophora brassicae is an endocellular parasite of cruciferous plants
It leads to the formation of galls containing mononucleate resting spores that occupy most of the cell [12, 26] (Fig. 1b, c)
Based on Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, we identified 171 proto-oncogenes that were implicated in the “Cancers” (Human Diseases) related pathways from the P. brassicae ZJ-1 genome, of which 46 genes were differentially expressed genes (DEGs) (Additional file 4: Table S2)

Summary

Introduction

The eukaryotic unicellular protist Plasmodiophora brassicae is an endocellular parasite of cruciferous plants. This protist develops a unicellular structure that is termed the plasmodium. The plasmodium is a multinucleated cell, which subsequently splits and forms resting spores. P. brassicae induces galls on the infected roots of cruciferous plants, such as oilseed rape and cabbage [3]. It severely disrupts the host root functions by inducing the formation of deformed galls, which reduce the uptake of water and nutrients from the soil and the growth of the roots [4]. P. brassicae forms primary plasmodia and primary zoosporangia in root hairs. The secondary zoospores are released from the broken root hairs and directly invade host cortical cells.

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