1508American Journal of Botany 91(10): 1508–1522. 2004.BIOLOGY AND SYSTEMATICS OF HETEROKONT ANDHAPTOPHYTE ALGAE1ROBERTA. ANDERSENBigelow Laboratory for Ocean Sciences, P.O. Box 475, West Boothbay Harbor, Maine 04575 USAIn this paper, I review what is currently known of phylogenetic relationships of heterokont and haptophyte algae. Heterokont algaeare a monophyletic group that is classified into 17 classes and represents a diverse group of marine, freshwater, and terrestrial algae.Classes are distinguished by morphology, chloroplast pigments, ultrastructural features, and gene sequence data. Electron microscopyand molecular biology have contributed significantly to our understanding of their evolutionary relationships, but even today classrelationships are poorly understood. Haptophyte algae are a second monophyletic group that consists of two classes of predominatelymarine phytoplankton. The closest relatives of the haptophytes are currently unknown, but recent evidence indicates they may be partof a large assemblage (chromalveolates) that includes heterokont algae and other stramenopiles, alveolates, and cryptophytes. Heter-okont and haptophyte algae are important primary producers in aquatic habitats, and they are probably the primary carbon source forpetroleum products (crude oil, natural gas).Key words: chromalveolate; chromist; chromophyte; flagella; phylogeny; stramenopile; tree of life.Heterokont algae are a monophyletic group that includes allphotosynthetic organisms with tripartite tubular hairs on themature flagellum (discussed later; also see Wetherbee et al.,1988, for definitions of mature and immature flagella), as wellas some nonphotosynthetic relatives and some that have sec-ondarily reduced or lost tripartite hairs. Brown seaweeds, di-atoms, and chrysophytes are commonly known members ofthe group. Haptophyte algae are a monophyletic group thatincludes all photosynthetic organisms with a haptonema, aswell as some nonphotosynthetic relatives, and some that havesecondarily lost the haptonema. The haptonema, from whichthe group derives its name, is a microtubule-supported ap-pendage that lies between two approximately equal flagella(for review, Inouye and Kawachi, 1994). The coccolithophoresand genera such as Pavlova and Isochrysis are commonlyknown members of the group. Representatives of heterokontalgae and haptophytes are shown in Figs. 1–24. Until 1992,haptophytes were included or closely aligned with heterokontalgae, but a nuclear small subunit ribosomal RNA (SSUrRNA) analysis indicated they are distantly related (Bhatta-charya et al., 1992). Recent molecular studies, based on othergenes, have now indicated that heterokont and haptophyte al-gae may be more closely aligned than the SSU rRNA dataindicated (Yoon et al., 2000a, b; Harper and Keeling, 2003;Ryall et al., 2003).Historical perspective—Brown seaweeds were referred toin early Chinese (ca. 3000 BC), Greek (e.g., Theophrastos, ca.300 BC), and Japanese (ca. 500 AD) writings, and knowledgeof brown seaweeds likely predated recorded history. In earlyhuman history, brown seaweeds were used for human and an-imal food, medicinal purposes, and dyes. Most other hetero-kont algae are microscopic, although mats of macroscopicVaucheria (Xanthophyceae) may have been known but notrecorded in historical works.The first modern scientific report is the description of Fucus1Manuscript received 31 December 2003; revision accepted 22 June 2004.I thank David Patterson and Hiroshi Kawai for providing color photographsof algae and Stacy Edgar for assistance with phylogenetic analysis. Supportedby NSF grants DEB-0206590 and DEB-0212138.E-mail: [email protected].(Phaeophyceae) by Linnaeus (1753), and shortly thereafter,microscopic chrysophytes (currently 5 Oikomonas, Anthophy-sa) were described by Mu¨ller (1773, 1786). The history ofheterokont algae was recently discussed in detail (Andersen,2004), and four distinct periods were identified. The discoveryperiod (1753–1882) is that era in which brown algae weredescribed as plants, and microalgae were described as infu-soria and treated as animals. Perhaps the most significant pub-lication of the era was the two-part publication of Ehrenberg(1838) that contained his light microscopic observations. Thefirst synthesis period (1882–1914) began when brown algaeand microalgae were first integrated and phylogenetic rela-tionships were discussed (Rostafinski, 1882; Correns, 1892;Klebs, 1893a, b; Lemmermann, 1899; Blackman, 1900), butthe period ended when these two groups were once again sep-arated (Pascher, 1914). The floristic period (1914–1950) wasdominated by the description of many species. There was anearly complete absence of evolutionary discussion, for theprimary reason that the light microscope was unable to resolvecharacters for determining relationships (Fritsch, 1935). Thesecond synthesis period (1950–2002) began with and wasdominated by evolutionary and phylogenetic relationships(e.g., Chadefaud, 1950; Bourrelly, 1957; Taylor, 1976; Leipeet al., 1996; Daugbjerg and Andersen, 1997a, b). Transmissionelectron microscopy provided a wealth of new and phyloge-netically informative data (e.g., Dodge, 1973; Hibberd, 1976;Taylor, 1976; Andersen, 1987), and biochemical studies werealso initiated (e.g., Strain, 1951; Quillet, 1955; Archibald etal., 1963; Ragan and Chapman, 1978; Smestad-Paulsen andMyklestad, 1978; Bjørnland and Liaaen-Jensen, 1989; Jeffrey,1989). Cladistic analysis brought new ways for analyzing evo-lutionary relationships (e.g., Hibberd, 1979; Lipscomb, 1989;Andersen, 1991; Williams, 1991; Sorhannus, 2001), and mo-lecular systematics added powerful new data sets (e.g., Gun-dersen et al., 1987; Leipe et al., 1994, 1996; Guillou et al.,1999b; Moriya et al., 2002; Goertzen and Theriot, 2003). Dis-coveries led to descriptions of many new taxa, including sev-eral classes: Eustigmatophyceae (Hibberd and Leedale, 1970),Dictyochophyceae (Silva, 1980), Synurophyceae (Andersen,1987), Coscinodiscophyceae and Fragilariophyceae (Round etal., 1990), Chrysomerophyceae (Cavalier-Smith et al., 1995),October 2004] 1509ANDERSEN—HETEROKONT AND HAPTOPHYTE ALGAEBolidophyceae (Guillou et al., 1999a), Pelagophyceae (Ander-sen et al., 1993), Phaeothamniophyceae (Bailey et al., 1998),Pinguiophyceae (Kawachi et al., 2002b), and Schizocladi-ophyceae (Kawai et al., 2003). The sequencing of the Thal-assiosira pseudonana genome, initiated in 2002, was thoughtto be the start of a
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