A census of nuclear cyanobacterial recruits in the plant kingdom.

Szabolcs Makai,Yuesheng Wang,Chuang Ma,Junli Chang,Javeed Hussain,Mingjie Chen,Guangyuan He,Zhaowan Yang,Guangxiao Yang,Cuiju Cui,Xiao Li,An-Yuan Guo,Yanhong Zhou

doi:10.1371/journal.pone.0120527

Abstract

The plastids and mitochondria of the eukaryotic cell are of endosymbiotic origin. These events occurred ~2 billion years ago and produced significant changes in the genomes of the host and the endosymbiont. Previous studies demonstrated that the invasion of land affected plastids and mitochondria differently and that the paths of mitochondrial integration differed between animals and plants. Other studies examined the reasons why a set of proteins remained encoded in the organelles and were not transferred to the nuclear genome. However, our understanding of the functional relations of the transferred genes is insufficient. In this paper, we report a high-throughput phylogenetic analysis to identify genes of cyanobacterial origin for plants of different levels of complexity: Arabidopsis thaliana, Chlamydomonas reinhardtii, Physcomitrella patens, Populus trichocarpa, Selaginella moellendorffii, Sorghum bicolor, Oryza sativa, and Ostreococcus tauri. Thus, a census of cyanobacterial gene recruits and a study of their function are presented to better understand the functional aspects of plastid symbiogenesis. From algae to angiosperms, the GO terms demonstrated a gradual expansion over functionally related genes in the nuclear genome, beginning with genes related to thylakoids and photosynthesis, followed by genes involved in metabolism, and finally with regulation-related genes, primarily in angiosperms. The results demonstrate that DNA is supplied to the nuclear genome on a permanent basis with no regard to function, and only what is needed is kept, which thereby expands on the GO space along the related genes.

Highlights

Plastids and mitochondria are plant organelles originally derived from endosymbiotic bacteria [1]
The numbers of nuclear-encoded proteins with putative cyanobacterial origin were, in all cases, greater than the numbers of nuclear encoded proteins homologous to plastid encoded proteins. This indicates the final stage of Endosymbiotic gene transfer (EGT), where the original genes are lost from the plastome
Arabidopsis had 585 nuclear encoded proteins of putative cyanobacterial origin, and 53 homologous to 27 plastid-encoded proteins, whereas only one plastid coded protein was homologous to putatively cyanobacterial protein encoded in the nucleus

Summary

Introduction

Plastids and mitochondria are plant organelles originally derived from endosymbiotic bacteria [1]. This DNA gains functionality by either retaining its original function or integrating into host-associated pathways [4,5,6] At this stage, an adequate mechanism for translocation of the protein product is required as a prerequisite [7,8,9,10,11,12]. A well-defined mechanistic model of this process was proposed for mitochondria, and the model shows that the process only stops when all coding DNA is transferred, which can lead to complete genome loss [14]. Such cases were reported in mitochondria [15]. The closest relative to modern-day plastids, Nostoc PCC 7120, has a genome of ~6.4 Mb which encodes ~5,400 proteins, whereas all sequenced plastomes encode only an average of 42–251 proteins [4, 17]

Methods

Results

Conclusion