Phylogenomic insights into the first multicellular streptophyte

Abstract

Streptophytes are best known as the clade containing the teeming diversity of embryophytes (land plants).^1,2,3,4 Next to embryophytes are however a range of freshwater and terrestrial algae that bear important information on the emergence of key traits of land plants. Among these, the Klebsormidiophyceae stand out. Thriving in diverse environments-from mundane (ubiquitous occurrence on tree barks and rocks) to extreme (from the Atacama Desert to the Antarctic)-Klebsormidiophyceae can exhibit filamentous body plans and display remarkable resilience as colonizers of terrestrial habitats.^5,6 Currently, the lack of a robust phylogenetic framework for the Klebsormidiophyceae hampers our understanding of the evolutionary history of these key traits. Here, we conducted a phylogenomic analysis utilizing advanced models that can counteract systematic biases. We sequenced 24 new transcriptomes of Klebsormidiophyceae and combined them with 14 previously published genomic and transcriptomic datasets. Using an analysis built on 845 loci and sophisticated mixture models, we establish a phylogenomic framework, dividing the six distinct genera of Klebsormidiophyceae in a novel three-order system, with a deep divergence more than 830 million years ago. Our reconstructions of ancestral states suggest (1) an evolutionary history of multiple transitions between terrestrial-aquatic habitats, with stem Klebsormidiales having conquered land earlier than embryophytes, and (2) that the body plan of the last common ancestor of Klebsormidiophyceae was multicellular, with a high probability that it was filamentous whereas the sarcinoids and unicells in Klebsormidiophyceae are likely derived states. We provide evidence that the first multicellular streptophytes likely lived about a billion years ago.

Keywords: Charophyta; ancestral character state; multicellularity; phylogenomics; plant evolution; plant terrestrialization; streptophyte algae.

Graphical abstract

Figure 1

Biogeography of Klebsormidiophyceae (A) World map with all the klebsormidiophycean strains used within this study. An interactive map can be accessed under https://tinyurl.com/yph2s4ma. (B) Details on the strains of Klebsormidiophyceae used in this study. (C) Cladogram of the genera in Klebsormidiophyceae. Dots label their distribution across climate zones, habitats, and body plan diversity. Character information was guided by Mikhailyuk et al.

Figure 2

A new three-order system of Klebsormidiophyceae based on phylogenomics (A) Maximum likelihood phylogenetic analyses based on 845 loci and the complex LG+C60 mixture model. UFBoot2 and an SH-like aLRT branch support test were employed. A dot labels full branch support; a colored halo around the dots labels the support indices for major clades. For additional assessment of robustness (gene jackknife and topology tests), see Figures S1B and S1C; a time-calibrated tree is shown in Figure S2. (B) A selection of the morphological diversity found across Klebsormidiophyceae. Scale bars are labeled in each of the micrographs.

Figure 3

Ancestral character state reconstruction of body plan and habitat characters across more than 800 million years of klebsormidiophycean evolution (A) To examine the ancestral character states of growth types in unicellular or multicellular organisms, coding schemes represented varying levels of complexity and hypotheses regarding the homology of growth types. The shown color-coded character state distributions represent yellow for unicellular growth and purple for multicellular growth sensu lato (including sarcinoid, filamentous, and parenchymatous growth). Note ancestor nodes for (1) Klebsormidiophyceae and Phragmoplastophyta 1008.4 million years ago (mya) and (2) Klebsormidiophyceae 830.8 mya. (B) To examine the ancestral habitats of the Klebsormidiophyceae, we coded habitat occurrences of the species as blue for aquatic and green for terrestrial. Note the terrestrial ancestor of Klebsormidiales, which lived 444.6 mya. Divergence dating is based on the molecular clock analyses shown in Figure S2. All ancestral character state reconstructions were done with a symmetric rates model because we consider most conservative by making the least assumptions about exchange rates; different coding schemes and asymmetric models are shown, alongside a key gene family salient to terrestrial adaptation (PAL), in Data S1.