Chloroplast Genome Traits Correlate With Organismal Complexity and Ecological Traits in Chlorophyta

Jiao Fang,Huan Zhu,Guoxiang Liu,Yangliang Chen,Heroen Verbruggen

doi:10.3389/fevo.2021.791166

Abstract

A positive relationship between cell size and chloroplast genome size within chloroplast-bearing protists has been hypothesized in the past and shown in some case studies, but other factors influencing chloroplast genome size during the evolution of chlorophyte algae have been less studied. We study chloroplast genome size and GC content as a function of habitats and cell size of chlorophyte algae. The chloroplast genome size of green algae in freshwater, marine and terrestrial habitats was differed significantly, with terrestrial algae having larger chloroplast genome sizes in general. The most important contributor to these enlarged genomes in terrestrial species was the length of intergenic regions. There was no clear difference in the GC content of chloroplast genomes from the three habitats categories. Functional morphological categories also showed differences in chloroplast genome size, with filamentous algae having substantially larger genomes than other forms of algae, and foliose algae had lower GC content than other groups. Chloroplast genome size showed no significant differences among the classes Ulvophyceae, Trebouxiophyceae, and Chlorophyceae, but the GC content of Chlorophyceae chloroplast genomes was significantly lower than that of Ulvophyceae and Trebouxiophyceae. There was a certain positive relationship between chloroplast genome size and cell size for the Chlorophyta as a whole and within each of three major classes. Our data also confirmed previous reports that ancestral quadripartite architecture had been lost many times independently in Chlorophyta. Finally, the comparison of the phenotype of chlorophytes algae harboring plastids uncovered that most of the investigated Chlorophyta algae housed a single plastid per cell.

Highlights

Viridiplantae split into the chlorophytes and streptophyta about a billion years ago (Zimmer et al, 2007; Morris et al, 2018)
Among the Ulvophyceae, chloroplast genomes of Bryopsidales and Ulvales are all smaller than 150 kb and at the other extreme are the Trentepohliales, with 6 of 7 chloroplast genomes exceeding 250 kb (Figure 2)
Compared with other IR-containing chloroplast genomes in Ulvophyceae, Trentepohlia odorata possessed a larger SSC region, which was caused by a long intergenic regions in SSC, and intergenic regions account for 69.2% of the SSC

Summary

Introduction

Viridiplantae split into the chlorophytes and streptophyta about a billion years ago (Zimmer et al, 2007; Morris et al, 2018). The streptophyta are comprised of land plants (embryophytes) and streptophyte algae (Fürst-Jansen et al, 2020). Many green algal chloroplast genomes feature a quadripartite architecture consisting of two inverted repeats and two single copies regions (Turmel et al, 1999, 2009; Lemieux et al, 2000). This structure is common in land plants (Luo et al, 2021) and has been shown in many species of the Chlorophyta as well. Quite a few green algae have a more traditional, larger and circular-mapping genome but lacking inverted repeat regions (de Cambiaire et al, 2007; Leliaert and Lopez-Bautista, 2015; Melton et al, 2015; Turmel et al, 2015, 2017; Cremen et al, 2018)

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