Parallel evolution of highly conserved plastid genome architecture in red seaweeds and seed plants.

Junmo Lee,Chung Hyun Cho,Seung In Park,John A West,Ji Won Choi,Hwan Su Yoon,Hyun Suk Song,Debashish Bhattacharya

doi:10.1186/s12915-016-0299-5

Junmo Lee, Chung Hyun Cho + Show 6 more

Open Access

https://doi.org/10.1186/s12915-016-0299-5

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Abstract

BackgroundThe red algae (Rhodophyta) diverged from the green algae and plants (Viridiplantae) over one billion years ago within the kingdom Archaeplastida. These photosynthetic lineages provide an ideal model to study plastid genome reduction in deep time. To this end, we assembled a large dataset of the plastid genomes that were available, including 48 from the red algae (17 complete and three partial genomes produced for this analysis) to elucidate the evolutionary history of these organelles.ResultsWe found extreme conservation of plastid genome architecture in the major lineages of the multicellular Florideophyceae red algae. Only three minor structural types were detected in this group, which are explained by recombination events of the duplicated rDNA operons. A similar high level of structural conservation (although with different gene content) was found in seed plants. Three major plastid genome architectures were identified in representatives of 46 orders of angiosperms and three orders of gymnosperms.ConclusionsOur results provide a comprehensive account of plastid gene loss and rearrangement events involving genome architecture within Archaeplastida and lead to one over-arching conclusion: from an ancestral pool of highly rearranged plastid genomes in red and green algae, the aquatic (Florideophyceae) and terrestrial (seed plants) multicellular lineages display high conservation in plastid genome architecture. This phenomenon correlates with, and could be explained by, the independent and widely divergent (separated by >400 million years) origins of complex sexual cycles and reproductive structures that led to the rapid diversification of these lineages.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0299-5) contains supplementary material, which is available to authorized users.

Highlights

The red algae (Rhodophyta) diverged from the green algae and plants (Viridiplantae) over one billion years ago within the kingdom Archaeplastida
We determined 17 novel red algal plastid genomes with three additional datasets derived from partial plastid genomes, bringing the total to 48 for this phylum. These genomes represent most red algal classes as well as the 12 orders of the largest subclass Rhodymeniophycidae (5011 species) in the class Florideophyceae (6755 species; see Algaebase: http://www.algaebase.org). With these broadly sampled genome data we asked the following two questions: what are the major trends in gene loss and endosymbiotic gene transfer (EGT) in these taxa, and what can we learn about the evolution of genome architecture following the ancient split of the red and green lineages within the Archaeplastida? Our results demonstrate extensive variation in algal plastid gene content and genome architecture but identify highly conserved plastid genomes in Florideophyceae and seed plants
The Stylonematophyceae, Porphyridiophyceae, and Compsopogonophyceae had intron-rich (38–65 introns) plastid genomes that distinguished them from other red algae

Summary

Introduction

The red algae (Rhodophyta) diverged from the green algae and plants (Viridiplantae) over one billion years ago within the kingdom Archaeplastida These photosynthetic lineages provide an ideal model to study plastid genome reduction in deep time. The donor lineage of these plastids remains relatively poorly studied, with only 29 plastid genomes reported, and these primarily from a single red algal class, the sexually reproducing (with one exception, see below) Florideophyceae, with no genomes available from three other classes that rely primarily on asexual reproduction (Stylonematophyceae, Compsopogonophyceae, and Rhodellophyceae) [6, 15,16,17,18,19,20,21,22,23,24,25,26,27] This imbalance in available data is readily apparent when compared to Viridiplantae, for which hundreds of complete plastid genomes have been determined. These “green” plastid genomes have been used to resolve basal group relationships in Viridiplantae and to document the high genome architecture variability in most green algae when compared to the extreme conservation found in flowering plants (about 800 genomes in GenBank) [28,29,30]

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