Dramatic Transcriptional Changes in an Intracellular Parasite Enable Host Switching between Plant and Insect

Kenro Oshima,Takuya Shiraishi,Kyoko Sugawara,Yasuyuki Yamaji,Nami Minato,Shigeyuki Kakizawa,Shigetou Namba,Misako Himeno,Yoshiko Ishii,Yutaro Neriya,Chihiro Miura

doi:10.1371/journal.pone.0023242

Abstract

Phytoplasmas are bacterial plant pathogens that have devastating effects on the yields of crops and plants worldwide. They are intracellular parasites of both plants and insects, and are spread among plants by insects. How phytoplasmas can adapt to two diverse environments is of considerable interest; however, the mechanisms enabling the “host switching” between plant and insect hosts are poorly understood. Here, we report that phytoplasmas dramatically alter their gene expression in response to “host switching” between plant and insect. We performed a detailed characterization of the dramatic change that occurs in the gene expression profile of Candidatus Phytoplasma asteris OY-M strain (approximately 33% of the genes change) upon host switching between plant and insect. The phytoplasma may use transporters, secreted proteins, and metabolic enzymes in a host-specific manner. As phytoplasmas reside within the host cell, the proteins secreted from phytoplasmas are thought to play crucial roles in the interplay between phytoplasmas and host cells. Our microarray analysis revealed that the expression of the gene encoding the secreted protein PAM486 was highly upregulated in the plant host, which is also observed by immunohistochemical analysis, suggesting that this protein functions mainly when the phytoplasma grows in the plant host. Additionally, phytoplasma growth in planta was partially suppressed by an inhibitor of the MscL osmotic channel that is highly expressed in the plant host, suggesting that the osmotic channel might play an important role in survival in the plant host. These results also suggest that the elucidation of “host switching” mechanism may contribute to the development of novel pest controls.

Highlights

IntroductionMalaria parasites can infect both human and mosquito vectors [1], and are rapidly transmitted by vectors over a wide area
Some pathogenic microorganisms can parasitise two quite different hosts
Global gene expression profiling To investigate gene expression levels for adaptation to diverse intracellular environments, the mRNA expression profiles of OYM grown in a plant or insect host were evaluated using microarray analysis

Summary

Introduction

Malaria parasites can infect both human and mosquito vectors [1], and are rapidly transmitted by vectors over a wide area Because this ‘‘host switching’’ is an essential stage in the life cycle of pathogens, it is important to determine its molecular mechanism(s) from the perspective of pest control. Phytoplasmas infect more than 700 plant species and bring about marked changes in plant development, including witches’ broom, dwarfism, and phyllody (Figure S1) [2,4]. Despite their economic importance and biological features, phytoplasmas remain the most poorly characterised plant pathogens, primarily because efforts at in vitro culture, gene delivery, and mutagenesis have been unsuccessful [3]

Methods

Results

Conclusion