Evolutionary Trends in the Mitochondrial Genome of Archaeplastida: How Does the GC Bias Affect the Transition from Water to Land?

Joan Pedrola-Monfort,Jose Soriano,Laia Pedrola,Carlos Boluda,Alfonso Garmendia,David Lázaro-Gimeno,Carla Soler

doi:10.3390/plants9030358

Abstract

Among the most intriguing mysteries in the evolutionary biology of photosynthetic organisms are the genesis and consequences of the dramatic increase in the mitochondrial and nuclear genome sizes, together with the concomitant evolution of the three genetic compartments, particularly during the transition from water to land. To clarify the evolutionary trends in the mitochondrial genome of Archaeplastida, we analyzed the sequences from 37 complete genomes. Therefore, we utilized mitochondrial, plastidial and nuclear ribosomal DNA molecular markers on 100 species of Streptophyta for each subunit. Hierarchical models of sequence evolution were fitted to test the heterogeneity in the base composition. The best resulting phylogenies were used for reconstructing the ancestral Guanine-Cytosine (GC) content and equilibrium GC frequency (GC*) using non-homogeneous and non-stationary models fitted with a maximum likelihood approach. The mitochondrial genome length was strongly related to repetitive sequences across Archaeplastida evolution; however, the length seemed not to be linked to the other studied variables, as different lineages showed diverse evolutionary patterns. In contrast, Streptophyta exhibited a powerful positive relationship between the GC content, non-coding DNA, and repetitive sequences, while the evolution of Chlorophyta reflected a strong positive linear relationship between the genome length and the number of genes.

Highlights

Mitochondrial, plastidial and nuclear genome lengths (GL) increased dramatically due to the addition of non-coding DNA (%NC) during the evolution of green plants, during the transition from water to terrestrial life
(Supplementary Table S1), the only significant relationship found was the one between the number of repeated sequences (NRS) and (Supplementary Table S1), the only significant relationship found was the one between the NRS and GL, with both logarithms transformed for linearity (Supplementary Materials Figure S1A)
Streptophyta lineage was removed from the analyses, and became more significant when the the Streptophyta lineage was removed from the analyses, and became more significant when the Chlorophyta lineage was the one excluded (Supplementary Materials Figure S1B,C)

Summary

Introduction

Mitochondrial, plastidial and nuclear genome lengths (GL) increased dramatically due to the addition of non-coding DNA (%NC) during the evolution of green plants, during the transition from water to terrestrial life. This phenomenon occurred in parallel with an increase in Guanine-Cytosine (GC) content (%GC) and organism complexity [1]. Green plants are further divided into two main clades: Chlorophyta, including most unicellular and marine algae; Streptophyta, including most freshwater algae and land plants [5] All these lineages have three genetic compartments with well-coordinated working biochemical machinery, and they differ significantly in their architecture and evolution [6]. Meaningful differences can be reflected in some of the mitochondrial genome (mtDNA) characteristics in the Archaeplastida lineages, such as the GLs, genetic code, codon usage, gene content, and the degree of ribosomal gene fragmentation [8]

Objectives

Methods

Results

Conclusion