A siphonous macroalgal genome suggests convergent functions of homeobox genes in algae and land plants

Abstract

Genome evolution and development of unicellular, multinucleate macroalgae (siphonous algae) are poorly known, although various multicellular organisms have been studied extensively. To understand macroalgal developmental evolution, we assembled the ∼26 Mb genome of a siphonous green alga, Caulerpa lentillifera , with high contiguity, containing 9,311 protein-coding genes. Molecular phylogeny using 107 nuclear genes indicates that the diversification of the class Ulvophyceae, including C. lentillifera , occurred before the split of the Chlorophyceae and Trebouxiophyceae. Compared with other green algae, the TALE superclass of homeobox genes, which expanded in land plants, shows a series of lineage-specific duplications in this siphonous macroalga. Plant hormone signalling components were also expanded in a lineage-specific manner. Expanded transport regulators, which show spatially different expression, suggest that the structural patterning strategy of a multinucleate cell depends on diversification of nuclear pore proteins. These results not only imply functional convergence of duplicated genes among green plants, but also provide insight into evolutionary roots of green plants. Based on the present results, we propose cellular and molecular mechanisms involved in the structural differentiation in the siphonous alga.

Differential gene expression in fronds and stolons of the siphonous macroalga, Caulerpa lentillifera

“…PP2Cs negatively regulate SnRK2 activity in land plants (Umezawa et al, ). However, these two gene families are highly expanded in the Caulerpa genome (Arimoto et al, ). Therefore, it is likely that each PP2C may suppress specific SnRK2s expressed in each structure, so that genes that are expressed in a given part might maintain structure‐specific signaling in the other part.…”

“…Our gene expression analysis was based on sequencing data obtained in the Caulerpa lentillifera genome decoding project (Arimoto et al, 2019). In that project, genomic DNA and mRNA of C. lentillifera F I G U R E 1 The siphonous green alga, Caulerpa lentillifera.…”

“…Plant hormones affect growth of macroalgae as they do land plants (Bradley, 1991;Evans & Trewavas, 1991;Lobban & Harrison, 1997). In addition, genomic data of Caulerpa lentillifera suggest that plant hormone-associated genes are expanded in this alga (Arimoto et al, 2019). Therefore, we further analyzed genes involved in plant hormone pathways.…”

“…In order to understand the biology of the siphonous body plan, we decoded the approximately 26‐Mb genome of C . lentillifera (Arimoto et al, ). This genome was estimated to contain 9,311 protein‐coding genes.…”

“…We focused on C. lentillifera, the size of which is similar to C. taxifolia, approximately 10 to 30 cm from stolon to frond apex ( Figure 1) (Paul, Neveux, Magnusson, & Nys, 2014;Ranjan et al, 2015). In order to understand the biology of the siphonous body plan, we decoded the approximately 26-Mb genome of C. lentillifera (Arimoto et al, 2019). This genome was estimated to contain 9,311 protein-coding genes.…”