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A Review of Auxospore Structure, Ontogeny and Diatom Phylogeny

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A Review of Auxospore Structure, Ontogeny and Diatom Phylogeny 16TH INTERNATIONAL DIATOM SYMPOSIUM, 25 AUG.-l SEPT. 2000, ATHENS & AEGEAN ISLANDS PROCEEDINGS 2001 (A. ECONOMOU - AMILLI, ED.), 601 PP., UNIVERSITY OF ATHENS, GREECE A review ofauxospore structure, ontogeny and diatom phylogeny I Kaczmarska, I., I Ehrman, J.M. and S.S. Bates 2 1. Department ofBio1ogy, Mount Allison University, Sack:ville, NB, E4L IG7, Canada 2. Fisheries and Oceans Canada, Gu1fFisheries Centre, P.O. Box 5030, Moncton, NB;EIC 9B6, Canada Abstract Interest in phylogenetic relationships within the diatoms has been recently rejuvenated by a number of reports based on the molecular approach that do not agree with the current phenetic phylogenies. Ontogeny has been successfully applied in studies of the evolutionary history of many animal and seed plants but has not been extensively tested with respect to diatoms. Here we propose such an approach. The literature indicates a considerable diversity in auxospore ontogeny and structure. Three basic types of auxospores occur: isometric (usually with siliceous scales in an organic wall), anisometric (with scales in the primary wall and a properizonium) and bilateral (with an organic· primary wall and a siliceous perizonium). These three types ofauxospores corroborate the recently developed molecular phylogeny of diatoms (Medlin et ai. 1997) where two major clades are apparent in this tree: Diatom Clade I (DC I) contains centric species with tubular processes located in most cases at the periphery of the valve. These diatoms produce isometric auxospores covered with scales. Clade 2 (DC2) consists of a diverse assemblage of diatoms, usually defined as multipolar centrics and pennates, and is divided into two sub-clades. The first (DsCzJ consists of mainly multipolar centrics with tubular processes located approximately at the center of the valve, and these diatoms produce anisometric auxospores with properizonia. The other (DsCZb) clusters pennate genera that produce bilateral auxospores with perizonia. Thisjntriguing correlation between the clades and auxospore types warrants further studies of auxospore fme structure. We suggest that auxospore ontogeny and structure may be useful characters in defining high level taxa such as classes or orders in a natural system ofdiatoms. Background Many studies have investigated the ongm of diatoms and the phylogenetic relationships among major lineages within the diatoms (e.g., Simonsen 1979, Round & Crawford 1981, Mann & Marchant 1989, Round et aI. 1990, Harwood & Gersonde 1990, Edlund & Stoermer 1997). In spite of this, neither aspect has yet been conclusively resolved, although considerable advances have been recently made in some areas using molecular techniques (Bhattacharya et aI. 1992, Medlin et aI. 1997b, Guillou et aI. 1999). Interest in phylogenetic relationships within the diatoms has been rejuvenated by several reports based on molecular approaches (Medlin et aI. 1993, Philippe et aI. -153- KACZMARSKA, I., EHRMAN, J.M. AND S.S. BATES 1994, Kooistra & Medlin 1996, Medlin et al. 1996a,b, Medlin 1997a), partially because these findings differ significantly from phenetic phylogenies that have prevailed in diatom literature for decades. Modem thinking about diatom evolution was initiated by Round & Crawford (1981, 1984), who hypothesized a monophyletic origin of diatoms and their phylogenetic connection to scale-bearing progenitors. This hypothesis is supported by molecular work where diatom monophyly is consistently shown by trees based on a variety of sequences (Bhattacharya et af. 1992, Medlin et aJ. 1997b, Daugbjerg & Anderson 1997, Van de Peer & De Wachter 1997, Guillou et aJ. 1999). Round et af. (1990, p. 122) pointed out how significant it would be to find scales in the gametes, and these have been recently found in the pennate diatom Pseudo-nitzschia multiseries (Hasle) Hasle (Kaczmarska et af. 2000) and possibly in oocytes ofActinocyclus sp. (Idei, pers. comm. 2000). Identifying the protoctistan ancestors of diatoms seems to be even more elusive. A close ancestry between diatoms and a number of heterokont taxa has been speculated over the last several decades: e.g., xanthophytes (Pascher 1921), Synurophyceae (Korshikov 1930, Round & Crawford 1989), parmalean algae (Mann & Marchant 1989), and lately, oomycetes (Schmid 1988, Leipe et af. 1994, Medlin et ai. 1997b, Sogin & Silberman 1998). Silica metabolism is present in all these groups (Bhattacharya et af. 1992), and some are diplobiontic and possess life-forms with scales. Recently, a molecular sister group of diatoms was serendipitously discovered among planktonic picobiflagellates (Guillou et af. 1999), clearly suggesting that microbial diversity has not yet been adequately researched foc a putative relative of diatoms. Phylogenetic relationships within the diatoms are equally difficult to unravel. Traditionally, valve symmetry, morphology and a few other characters (e.g., cytological, reproductive) were used to infer evolutionary rebdedness among the taxa. Most broadly accepted modem systems were developed by Hustedt (1930-1966), Simonsen (1979) and Round et ai. (1990). All these systems adopted basically a view of diatom diversity that supported Schutt's distinction between radially symmetric Centrics and bilateral Pennates. Different systematic ranks have been given to these two groups, commonly either classes or orders, e.g., Centra1es and Pennales. This distinction was substantiated by two modes of sexual reproduction, oogamy in centric and isogamy in pennate diatoms. However, this system was not universally accepted (Hendey 1964, Patrick & Reimer 1960). Somewhat earlier, pa1aeodiatomists working in the former Soviet Union collectively erected a third taxon, Mediales, to accommodate many fossil diatoms whose valve symmetry and morphology could not be reconciled with the systematic division ofdiatoms into the two orders Centrales and Pennales (Proshkina-Lavrenko 1949-1950). Many ofthe taxa assigned to the Mediales were species with a non-circular valve outline but with a radial pattern of valve ornamentation. Ontogeny has been successfully applied in studies ofthe evolutionary history ofmany animals and seed plants. The feasibility of this approach has not been extensively tested with diatoms, although it has already been postulated by Kociolek & Williams -154- AUXOSPORE STRUCTURE, ONTOGENY AND DIATOM PHYLOGENY (1987). Here, we theorize on the significance of auxospore ontogeny in reconstructing phylogenetic relationships within diatoms and suggest such an approach to identitY their majorJineages. We fir~t summarize the observations on auxospore structure and development (based on a review of the literature and on our own research), and then place this information within the context of classical diatom systematics, contrasting this with what is currently known about the molecular phylogeny ofdiatoms. Definition ofterms Although some ofthe following terms are defined in several publications (Anonymous 1975, Ross et al. 1979, Stosch 1982, Round et al. 1990, Kaczmarska et al. 2000), they may not be obvious to all readers. Here, we define these terms as they are used in this paper. 1. Zygote: a cell with a diploid nucleus resulting from fusion oftwo gametes. 2. Auxospore: a cell destined to restore large size individuals in a diatom population. Depending on species and the stage of development, the auxospore may contain one diploid nucleus (zygote) or two haploid nuclei (dikaryon state). In addition, in some auxospores a varying number ofpycnotic nuclei may also be present. 3. Cell wall: protective layer external to the plasma membrane. Here, cell wall is used interchangeably with the term cell envelope. 4. Properizonium: a secondary auxospore wall, built of siliceous rings produced inside and coalescent with the primary, scaly wall (Stosch 1982). These bands, rings, loops or hoops are laid at various orientation relative to the direction of the initial valve expansion. 5. Perizonium: secondary wall of the bilateral auxospore consisting of closed or open rings laid at fixed orientation relative to the direction ofinitial valve expansion. 6. Isometric auxospores: auxospores with a dilatable cell wall, normally containing scales of various size and shape (sometimes even elongated); covering the entire surface area ofa usually spherical cell. 7. Anisometric auxospores: auxospores with partitioned walls, one part (primary) containing scales, the other (secondary) properizonium; the scaly wall and properizo­ nium each cover different areas ofthe protoplast. 8. Bilateral auxospores: auxospores with perizonia and sometimes with scales. 9. Initial valves: valves produced within the auxospore, may number 2-5, depending on species. 10. Initial frustule: first two valves produced within the auxospore. 11. Initial cell: cell liberated from the auxospore and capable of at least one mitotic ---\. division outside the auxospore. Initial cell mayor may not contain an initial frustule. 12. Auxospore ontogeny: a development of auxospore from fertilization (plasmogamy ofgametes) to maturity (immediately prior to liberation ofinitial cell). -155- KACZMARSKA, I., EHRMAN, lM. AND S.S. BATES Auxospore structure and development The auxospore is unique to the diatoms. Most commonly the cell results from allogamOlis fusion, and its major function in diatom life history is to restore the larger sizes in a vegetatively propagating population. Typically the auxospore cell wall consists oftwo biogenic constituents: organic matter and siliceous elements, though the relationships between
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