Resurrection of the Family Grateloupiaceae Emend. (Halymeniales, Rhodophyta) Based on a Multigene Phylogeny and Comparative Reproductive Morphology

Su Yeon Kim,Hyung Woo Lee,Myung Sook Kim,Juan Lopez-Bautista,Sung Min Boo,Eun Chan Yang,Hwan Su Yoon,Suzanne Fredericq,Roberta D’Archino

doi:10.3389/fevo.2021.775627

Abstract

The marine red algal order Halymeniales currently includes two families, the Halymeniaceae and Tsengiaceae, and consist of 38 genera and about 358 species. Phylogenetic analyses on specific taxa of the order are common, but not comprehensive, leaving the many intra-ordinal relationships within the Halymeniales unresolved. To reassess the phylogeny of the Halymeniales, we conducted extensive phylogenetic analyses based on 207 rbcL sequences and multigene analyses (rbcL, psaA, psbA, cox1, and LSU) using 47 taxa from the order. The combined data set fully supports the monophyly of the Grateloupia sensu lato clade. Phylogenetic assessment of the reproductive structures in the order using the type of auxiliary cell ampullae, pericarp origin, and tetrasporangial development characters, supports a Grateloupia sensu lato clade distinct from the Halymeniaceae exemplified by the generitype Halymenia. As a result, we propose to reinstate the family Grateloupiaceae Schmitz based on the Grateloupia sensu lato clade and including Grateloupia and eight other genera: Dermocorynus, Mariaramirezia, Neorubra, Pachymeniopsis, Kintokiocolax, Phyllymenia, Prionitis, and Yonagunia. The emended Grateloupiaceae is distinguished from the Halymeniaceae by the following three characteristics; (i) simple unbranched and unilateral type of auxiliary cell ampullae, (ii) pericarp formed densely by the fusion of secondary medullary filaments from subcortical cells and lateral ampullary filaments from a fusion cell complex, (iii) tetrasporangia originating laterally from the outer cortex. The Halymeniales comprises the monophyletic Grateloupiaceae, Halymeniaceae sensu lato (which requires further study), and the Tsengiaceae.

Highlights

The monophyletic Rhodophyta has been divided into seven classes based on multigene data (Yoon et al, 2006)
The Grateloupia sensu lato clade was comprised of nine genera: Pachymeniopsis, Kintokiocolax, Prionitis, Neorubra, Phyllymenia, Grateloupia, Yonagunia, Dermocorynus, and Mariaramirezia
We consider that the resurrection of the monophyletic Grateloupiaceae is a first step toward resolving the Halymeniales with the aim of adapting the classification system based on genetic monophyly

Summary

Introduction

The monophyletic Rhodophyta has been divided into seven classes based on multigene data (Yoon et al, 2006). A series of molecular phylogenetic studies by Saunders et al (2002), Withall and Saunders (2006), and Le Gall and Saunders (2007) provided many improvements for resolving relationships among florideophyte orders. The close relationships of Halymeniales, Sebdeniales, and Rhodymeniales were confidently resolved based on multigene and mitochondrial genome data (e.g., Yang et al, 2015, 2016). In 1996 Saunders and Kraft recognized a new name, the Halymeniales, for the red algal order that was previously known as the Cryptonemiales Kylin, based on small-subunit rRNA phylogenetic analyses. C. Fan from the Nemastomatales to the Halymeniales with the establishment of the new monogeneric family Tsengiaceae. In the current molecular taxonomic framework, the order Halymeniales includes two families, the Halymeniaceae and Tsengiaceae, consisting of 38 genera and about 358 species (Guiry and Guiry, 2021)

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