Nuclear genome of a pedinophyte pinpoints genomic innovation and streamlining in the green algae

Abstract

Summary The genomic diversity underpinning high ecological and species diversity in the green algae (Chlorophyta) remains little known. Here, we aimed to track genome evolution in the Chlorophyta, focusing on loss and gain of homologous genes, and lineage‐specific innovations of the core Chlorophyta. We generated a high‐quality nuclear genome for pedinophyte YPF701, a sister lineage to others in the core Chlorophyta and incorporated this genome in a comparative analysis with 25 other genomes from diverse Viridiplantae taxa. The nuclear genome of pedinophyte YPF701 has an intermediate size and gene number between those of most prasinophytes and the remainder of the core Chlorophyta. Our results suggest positive selection for genome streamlining in the Pedinophyceae, independent from genome minimisation observed among prasinophyte lineages. Genome expansion was predicted along the branch leading to the UTC clade (classes Ulvophyceae, Trebouxiophyceae and Chlorophyceae) after divergence from their last common ancestor with pedinophytes, with genomic novelty implicated in a range of basic biological functions. Results emphasise multiple independent signals of genome minimisation within the Chlorophyta, as well as the genomic novelty arising before diversification in the UTC clade, which may underpin the success of this species‐rich clade in a diversity of habitats.

The origin and early evolution of plants

“…Within the chlorophytes, prasinophytes (e.g., Chlorodendrophyceae, Nephroselmidophyceae, Mamiellophyceae) have usually been considered to comprise a clade, but their relationships are disputed. Phylogenomic analyses suggest that prasinophytes are paraphyletic and comprise successive sister lineages to the core chlorophytes (Figure 2) [11,22,27]. The ancestor of Chlorophyta likely diversified in marine environments, leading to the evolution of the core chlorophytes that subsequently radiated into marine, freshwater, and terrestrial environments [11,28].…”

Alexander Bowles

“…As an evolutionary plant biologist, I have enjoyed recent works on land plant evolution (de Vries & Archibald, 2018), the anatomy and evolution of lycopsid rooting structures (Hetherington & Dolan, 2016), the evolutionary success of ferns (McElwain, 2011) and discussion on the need for more nonseed plant model organisms (Rensing, 2017). Some of my favourite research papers include: studies by Xu et al (2022) and Repetti et al (2022) of the genome of Pedinomonas minor, identifying the genomic evolution of chlorophytes; analysis by Clark et al (2016) of the evolution of fern genome traits; the work by Barba-Montoya et al (2018) to constrain the timing of the diversification of angiosperms; and that of Brockington et al (2015) which found that lineage-specific radiations of key biosynthetic genes explain betalain pigmentation in the flowering plant order Caryophyllales. All of these inspiring works have helped to stimulate ideas and discussion, as well as providing excellent reviews of the literature.…”

“…(2022) and Repetti et al . (2022) of the genome of Pedinomonas minor , identifying the genomic evolution of chlorophytes; analysis by Clark et al . (2016) of the evolution of fern genome traits; the work by Barba‐Montoya et al .…”

Dollo parsimony overestimates ancestral gene content reconstructions

“…One of the most frequent applications of Dollo parsimony has been in reconstructing the gains and losses of genes in the lineages leading to major multicellular eukaryotic groups, including land plants (Bowles et al, 2020), animals (Fairclough et al, 2013; Najle et al, 2023; Paps & Holland, 2018), and brown algae (Cock et al 2010). It has been applied to examine patterns of gene gain and loss in the evolution of novel trophic modes or in the adaptation to specific environments in fungi and their relatives (Mikhailov et al 2017, Galindo et al, 2018, Galindo et al 2021, Mikhailov et al 2022), in green algae (Repetti et al 2022), and in red algae (Cho et al 2023). Dollo parsimony has also been employed to investigate the evolution of gene gains and losses that may have led to physiological changes such as those underlying the evolution of Wolffia australiana , the smallest known flowering plant (Park et al, 2021).…”