Regulation of chloroplast and nucleomorph replication by the cell cycle in the cryptophyte Guillardia theta

Ryo Onuma,Neha Mishra,Shin-Ya Miyagishima

doi:10.1038/s41598-017-02668-2

Abstract

The chloroplasts of cryptophytes arose through a secondary endosymbiotic event in which a red algal endosymbiont was integrated into a previously nonphotosynthetic eukaryote. The cryptophytes retain a remnant of the endosymbiont nucleus (nucleomorph) that is replicated once in the cell cycle along with the chloroplast. To understand how the chloroplast, nucleomorph and host cell divide in a coordinated manner, we examined the expression of genes/proteins that are related to nucleomorph replication and chloroplast division as well as the timing of nuclear and nucleomorph DNA synthesis in the cryptophyte Guillardia theta. Nucleus-encoded nucleomorph HISTONE H2A mRNA specifically accumulated during the nuclear S phase. In contrast, nucleomorph-encoded genes/proteins that are related to nucleomorph replication and chloroplast division (FtsZ) are constantly expressed throughout the cell cycle. The results of this study and previous studies on chlorarachniophytes suggest that there was a common evolutionary pattern in which an endosymbiont lost its replication cycle-dependent transcription while cell-cycle-dependent transcriptional regulation of host nuclear genes came to restrict the timing of nucleomorph replication and chloroplast division.

Highlights

Chloroplasts trace their origin to a primary endosymbiotic event in which an ancestral cyanobacterial endosymbiont was reduced into the chloroplast
In primary algae and land plants, chloroplast division is performed by the constriction of a macromolecular ring-like division machinery that is comprised of a self-assembling GTPase FtsZ of cyanobacterial endosymbiotic origin and another, self-assembling GTPase dynamin (DRP5B) of eukaryotic host origin[8, 9]
The aim of this study was to characterise the relationship between the progression of the host cell cycle, timing of nucleomorph replication and timing of chloroplast division

Summary

Introduction

Chloroplasts trace their origin to a primary endosymbiotic event in which an ancestral cyanobacterial endosymbiont was reduced into the chloroplast (the primary chloroplast surrounded by the inner and the outer envelope membranes). During the course of the establishment of these secondary chloroplasts, most of the eukaryotic algal endosymbiont cellular compartments other than the chloroplast and plasma membrane had been lost. Other secondary algae have completely lost the nuclei of endosymbionts[2, 3] The continuity of both primary and secondary chloroplasts is maintained by chloroplast division in eukaryotic host cells. In primary algae and land plants, chloroplast division is performed by the constriction of a macromolecular ring-like division machinery that is comprised of a self-assembling GTPase FtsZ of cyanobacterial endosymbiotic origin and another, self-assembling GTPase dynamin (DRP5B) of eukaryotic host origin[8, 9]. DRP5B is recruited to the cytosolic side of the division site and the competent chloroplast division machinery begins to constrict[8, 9]

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