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Molecular Phylogenetics and Evolution 52 (2009) 329–339

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Molecular Phylogenetics and Evolution 52 (2009) 329–339 Molecular Phylogenetics and Evolution 52 (2009) 329–339 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogenetic relationships and species circumscription in Trentepohlia and Printzina (Trentepohliales, Chlorophyta) Fabio Rindi *, Daryl W. Lam, Juan M. López-Bautista Department of Biological Sciences, The University of Alabama, P.O. Box 870345, 425 Scientific Collections Bldg., Tuscaloosa, AL 35487-0345, USA article info a b s t r a c t Article history: Subaerial green microalgae represent a polyphyletic complex of organisms, whose genetic diversity is Received 28 October 2008 much higher than their simple morphologies suggest. The order Trentepohliales is the only species-rich Revised 12 January 2009 group of subaerial algae belonging to the class Ulvophyceae and represents an ideal model taxon to inves- Accepted 15 January 2009 tigate evolutionary patterns of these organisms. We studied phylogenetic relationships in two common Available online 7 February 2009 genera of Trentepohliales (Trentepohlia and Printzina) by separate and combined analyses of the rbcL and 18S rRNA genes. Trentepohlia and Printzina were not resolved as monophyletic groups. Three main clades Keywords: were recovered in all analyses, but none corresponded to any trentepohlialean genus as defined based on 18S rRNA gene morphological grounds. The rbcL and 18S rRNA datasets provided congruent phylogenetic signals and Chlorophyta Molecular systematics similar topologies were recovered in single-gene analyses. Analyses performed on the combined 2-gene Morphological convergence dataset inferred generally higher nodal support. The results clarified several taxonomic problems and Printzina showed that the evolution of these algae has been characterized by considerable morphological conver- rbcL gene gence. Trentepohlia abietina and T. flava were shown to be separate species from T. aurea; Printzina lage- Subaerial algae nifera, T. arborum and T. umbrina were resolved as polyphyletic taxa, whose vegetative morphology Substitutional saturation appears to have evolved independently in separate lineages. Incongruence between phylogenetic rela- Trentepohlia tionships and traditional morphological classification was demonstrated, showing that the morphological Trentepohliales characters commonly used in the taxonomy of the Trentepohliales are phylogenetically irrelevant. Ulvophyceae Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction 2007). A direct consequence of this phenomenon is that the classi- fication at the genus and species level requires a reassessment Subaerial green microalgae are among the most widespread and based on a polyphasic combination of different approaches (Prösc- evolutionarily diverse organisms inhabiting terrestrial environ- hold and Leliaert, 2007). At present, the limited amount of DNA se- ments. Their systematics have been traditionally problematic and quence data available for most groups is the main hurdle to the surrounded by great controversy. In the past, their classification completion of such a reassessment. was entirely based on morphological characters (Smith, 1950; Ettl The order Trentepohliales is an ideal model taxon to illustrate and Gärtner, 1995). However, since the morphology of most spe- the complexity of the problems that affect the systematics and tax- cies is unicellular and affected by great plasticity, the set of reliable onomy of subaerial green algae. This order includes microchloro- characters useful for systematic purposes is limited. In the last phytes occurring in a wide range of habitats in areas with humid 15 years, DNA sequence data have become gradually available and rainy climates. Although most diverse and abundant in tropical and have led to important insights into the evolution of these regions, the Trentepohliales are also found in temperate zones and organisms. It has become clear that terrestrial green algae are a occur on a large variety of substrata, such as bark, leaves and fruits highly polyphyletic group originating from colonization of terres- of vascular plants, wood, metal, plastic, stones and concrete trial environments by many separate lineages of aquatic (both (Thompson and Wujek, 1997; López-Bautista et al., 2002; Rindi freshwater and marine) algae (Huss et al., 1999; Lewis and and López-Bautista, 2007). They are also among the most common McCourt, 2004; Lewis and Lewis, 2005; Watanabe et al., 2006; Le- phycobionts in lichens (Chapman and Good, 1983; Nakano and wis, 2007; Cardon et al., 2008). The adaptation to a terrestrial life- Ihda, 1996; Chapman and Waters, 2001). When present in large style has resulted into a convergent morphology in algae belonging amounts, their occurrence is revealed by the red, orange or yellow to widely separated evolutionary lineages (López-Bautista et al., color produced by the accumulation of carotenoids in their cells. The order contains the single family Trentepohliaceae and is distin- guished from all other green algae by the combination of the fol- * Corresponding author. Present address: Martin Ryan Institute, National Uni- versity of Ireland, Galway, Ireland. Fax: +353 91 525005. lowing features: presence of b-carotene and haematochrome; E-mail address: [email protected] (F. Rindi). absence of pyrenoids in the chloroplast; flagellar apparatus with 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.01.009 330 F. Rindi et al. / Molecular Phylogenetics and Evolution 52 (2009) 329–339 unique ultrastructure (described in detail by Chapman and Henk, of variation between different character states in the same spe- 1983 and Roberts, 1984); transverse cell walls with plasmodes- cies, sometimes in the same specimen. Some species of Tren- mata; and presence of a characteristic reproductive structure, the tepohlia and Printzina are characterized by great plasticity sporangiate lateral (a highly modified branch consisting of an api- related to environmental factors, and their morphology may cal cell that is swollen basally and tapers apically into a short neck, vary considerably depending on the environmental conditions on which a spherical or oval zoosporangium is borne). (Howland, 1929; Nakano and Handa, 1984; Thompson and Wu- This unusual combination of characters has been a source of jek, 1997; Rindi and Guiry, 2002). As in other groups of ulvo- great confusion in the classification of the Trentepohliales at all phycean green algae (i.e., Verbruggen et al., 2007a; De Clerck taxonomic levels, in particular the class level. The possible inclu- et al., 2008), there are extensive ‘‘grey” zones between tradi- sion of these algae in at least three different classes was suggested tional species defined on morphology. Collection of specimens in the past (López-Bautista and Chapman, 2003, and references for which the morphology does not correspond satisfactorily therein), as well as the elevation to the rank of a class, the Tren- to any of the species currently included in these genera is a tepohliophyceae (Van den Hoek et al., 1995). López-Bautista and common situation in field investigations, and for this reason Chapman (2003) provided robust evidence for placement in the species of Trentepohlia are often identified at the genus level, class Ulvophyceae based on 18S rRNA sequence data. The molecu- sometimes only at family or order level. Another factor that lar evidence currently available suggests that the Trentepohliales greatly complicates taxonomic matters is the fact that several form a well-supported monophyletic group sister to a clade com- species were described by early authors, who provided only a posed of the order Dasycladales and the clade Cladophorales– very vague description (Linnaeus, 1753, 1759; Agardh, 1824; Siphonocladales (López-Bautista and Chapman, 2003). Kützing, 1843; Zeller, 1873); for some of them, no type speci- At the genus level, the classification of the Trentepohliales has mens or other authentic specimens are available (i.e., Trentepoh- been traditionally based on the scheme proposed by Printz lia aurea and T. iolithus). For this reason, the identity of some (1939). In this monograph, five genera (Cephaleuros, Phycopeltis, species has become very confused in the course of the time, Physolinum, Stomatochroon, Trentepohlia) were recognized on mor- and the circumscription of several morphologically similar taxa phological basis. Cephaleuros Kunze includes 17 species and con- remains to this day an unsolved matter. sists of filaments irregularly branched, free or coalescent to DNA sequence data for the Trentepohliales have become avail- produce irregular discs that grow below the cuticle or the epider- able relatively recently (López-Bautista and Chapman, 2003; mis of leaves of vascular plants. Species of Phycopeltis Millardet López-Bautista et al., 2003, 2006). López-Bautista et al. (2006) is consist of creeping filaments, usually coalescing to produce more thus far the only study that has considered the phylogeny of the or less regular discs epiphytic on leaves, stems and fruits of vascu- Trentepohliales at the genus and species level using molecular data lar plants; the genus currently includes 26 species. Stomatochroon (18S rRNA gene sequences). This investigation suggested a lack of Palm includes four species with diminutive habit, growing in correspondence between molecular phylogeny and traditional leaves of vascular plants as filamentous endophytes, the presence classification based on morphological
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