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Atypical Development of Chaetomorpha Antennina in Culture (Cladophorales, Chlorophyta)

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Atypical Development of Chaetomorpha Antennina in Culture (Cladophorales, Chlorophyta) Phycological Research Phycological Research 2011; 59: 91-97 Atypical development of Chaetomorpha antennina in culture (Cladophorales, Chlorophyta) Frederik Leliaert,* Sofie D’hondt, Lennert Tyberghein, Heroen Verbruggen and Olivier De Clerck Phycology Research Group, Biology Department, Ghent University, Ghent, Belgium for vague boundaries in several species (Leliaert & SUMMARY Boedeker 2007). However, some species are clearly circumscribed and exhibit a fairly constant morphology The green seaweed genus Chaetomorpha is character­ throughout their ecological and geographical range, for ized by unbranched filaments. Molecular phylogenetic exam ple C. an te n n in (Bory a de Saint-Vincent) Kützing, data indicate that Chaetomorpha forms a clade that C. m o n ilig e ra Kjellman, C. robusta (Areschougi Papen- is nested in a paraphyletic assemblage of branched fuss, C. sp ira lis Okamura and C. v ie illa rd ii(Kützing) species ( C ladophora). It follows that the unbranched Wynne. condition is evolutionarily conserved and likely evolved Chaetomorpha antennina has a pantropical distribu­ early in the evolution of this clade. In this study we tion and is easily identifiable by its characteristic erect, show that under laboratory culture conditions, the fila­ brush-like tufts, composed of straight, rigid filaments m ents of C. an te n n in afrequently produce lateral borne on a long clavate basal cell with annular constric­ branches, similar to Cladophora. Our results thus indi­ tions (Bprgesen 1913; Abbott & Hollenberg 1976; cate that the unbranched thai lus architecture is not Abbott & Huisman 2004; Coppejans e t al. 2005; Kraft entirely genetically constrained, but at least in part 2007; Coppejans e ta !. 2009). The species typically subject to morphological plasticity. Additionally, culture grows on intertidal to shallow subtidal rocks that are observations of C. an te n n in aallowed a detailed study surf-exposed or subject to strong surge. The plants of rhizoidal development, which seems unique among firmly attach by rhizoids developing from the proximal Cladophorales. pole of the basal cells, resulting in a profusely branched, stoloniferous rhizoidal system. Key words: culture, green algae, morphological devel­ In this paper we describe atypical development of C. opment, phenotypic plasticity. a n te n n in aunder laboratory culture conditions, includ­ ing formation of branches in the upright filaments. Culture observations also allowed a detailed study of the development of the stoloniferous rhizoidal system in INTRODUCTION this species. Chaetomorpha is a common and widespread green seaweed genus, characterized by unbranched fila­ MATERIALS AND METHODS ments. Molecular phylogenetic data indicate that Chaetomorpha antennina plants were collected along Chaetomorpha forms a clade, which is nested in the Pacific coast of Mexico (Table 1). Portions of each a paraphyletic assemblage of branched Cladophora specimen were preserved in 5% formalin in seawater, species (Leliaert e ta !. 2009). This suggests that the dried in silica gel, and kept alive in seawater. After unbranched filamentous architecture evolved from thalli were transferred to fresh seawater in the lab, branched forms early in the evolution of the C haeto­ sporangia developed within 1-2 weeks, and unialgal m orpha clade and that this morphological character cultures were established by isolation of spores. Algal likely has a strong genetic basis. It should be noted, cultures were grown in sterile lx modified Provasoli however, that apart from Chaetomorpha, unbranched enriched seawater (West 2005) under ‘high’ and ‘low’ forms have evolved several times independently in the light intensity (25-30 and 5-10 pE n r 2 s_1) and ‘h ig h ’ Cladophorales, i.e. in a clade containing Rhizoclonium rip a riu m (Roth) Harvey and in R. africanum K ützing (Le lia ert e t al. 2 0 0 9 ). A bo ut 5 0 Chaetomorpha species are currently rec­ *To whom correspondence should be addressed. ognized based on a few morphological features, such as Email: frederik. Ieliaert@ugent. be growth form, cell dimensions and shape of the basal Communicating editor: G. H. Kim. attachment cell. The scarcity of diagnostic characters, Received 6 May 2010; accepted 29 October 2010. combined with ecologically induced variations accounts doi: 10. I l l 1/j. 1440-1835.2010.00604.x © 2011 Japanese Society of Phycology 92 F. Leliaert et al. Table 1. Specimens from which partial large subunit (LSU) nrDNA sequences were newly determined Species Collection information EMBL accession numbers Chaetomorpha GUAM117, Guam: Talofofo Bay (Sehlis T., 23 Jul. 2007) FN687234 antennina C. antennina GUAM118, Guam: Talofofo Bay (Schils T., 23 Jul. 2007) FN687235 C. antennina HEC15206, Madagascar : Tolanaro: Plage de Libanona, wave-exposed intertidal rocky flat (Coppejans FN687236 E., 3 0 Aug. 2 0 0 2 ) C. antennina KZN2047, South Africa: Kwazulu-Natal: Palm Beach, intertidal (Leliaert F., 7 Feb. 2001) FN687237 C. antennina KZN2322, South Africa (Indian Ocean): Kwazulu-Natal: Durban: Isipingo (Leliaert F., 16 Jun. 2003) FN687238 C. antennina MX0172, Mexico (Pacific Ocean): Guerrero: Acapulco: Canal de Boca Chica: Isla Roqueta, exposed FN687239 intertidal rock on vertical wall facing ocean (Verbruggen H. & Tyberghein L., 19 Feb. 2009) C. antennina MX0220, Mexico (Pacific Ocean): Guerrero: Ixtapa: Playa del Palmar, on seaward side of intertidal FN687240 rock boulder on the beach (Verbruggen H. & Tyberghein L., 21 Feb.2009) C. antennina MX0275, Mexico (Pacific Ocean): Colima: Manzanillo: Playa la Audiencia, intertidal wave channel, FN687241 exposed to heavy wave action (Tyberghein L. & Verbruggen H., 23 Feb. 2009) C. gracilis HEC12944, Tanzania: Mtwara: Mana Hawanja, intertidal rock flat; shallow pool (Coppejans E., 29 FN687242 Jul. 2 0 0 0 ) Chaetomorpha sp.Bunkerö, United Kingdom: Wales: Pembrokeshire: Milford Haven, on maerl, 2-4 m deep (Bunker F., FN687243 6 Nov. 2 0 0 7 ) Chaetomorpha sp.HV709, Philippines: Bohol: Panglao, sandy intertidal flat, loosely attached to a seagrass (Verbruggen FN687244 H., 1 Feb. 2 0 0 4 ) Rhizoclonium FL703, Tanzania: Zanzibar: Nungwi, su pra I ¡tora I, epilithic (Leliaert F., 26 Jul. 1997) FN687245 africanum and ‘low’ temperature (23°C and 17°C). Cultures were - KZN2322 - KZN2047 not shaken or aerated. Photographs were taken with a GUAM 117 GUAM118 ColorView (Olympus) digital camera mounted on an MX0275 Chaetomorpha antennina Olympus BX51 bright field microscope or Olympus f H EC 15206 rMX0172 T- MX0220 _ SZX10 stereo microscope (Olympus Co., Tokyo, Japan). i C. linum HV709 1 00 i— C. crassa AJ544767 Morphology-based species identification was verified I C.Í spiralis AJ544766 by sequencing the variable C1D2 region of the large C. aerea F M 205025 C. sp. Bunkers subunit (LSU) nrDNA of the Mexican plants (field- QQ i C. sp. AJ544758 I i! L o o i- C. brachygona AJ544759 collected specimens and cultures) along with additional L C. gracilis HEC 12944 ■ Chaetomorpha norvegica FN257509 specimens of C. an te n n in from a South Africa, Madagas­ ■ Chaetomorpha melagonium FN257511 • Rhizoclonium riparium AJ544765 car and Guam (Table 1). DNA extraction, polymerase ■ Cladophora vagabunda AM503481 ■ Cladophora rupestris AJ544764 chain reaction (PCR) amplification and sequencing were - Rhizoclonium africanum FL703 ■ Cladophora ordinata AJ544757 performed as described in Leliaert e ta !. (2007). The ■ Cladophora pellucida FM205036 - Cladophora pygmaea FM205040 newly generated sequences were combined with avail­ —\ able sequences from 10 Chaetomorpha species and other representatives of the C ladophora clade (as cir­ Fig. 1. Bayesian phylogenetic tree inferred from partial large cumscribed by Leliaert e ta !. 2009). Sequences were subunit (LSU) nrDNA sequences, showing possible monophyly of aligned using MUSCLE (Edgar 2004), and visually Chaetomorpha, and all C. antennina specimens clustering in a inspected. The dataset was analyzed with Bayesian well supported clade of closely related sequences. inference (Bl), using MrBayes v3.1.2 (Ronquist & Huelsenbeck 2003), under a GTR+G model as deter­ mined by the Akaike Information Criterion in JModeltest preceded by a well supported branch, confirming the vO.1.1 (Posada 2008). The analysis consisted of 4 morphology-based species identifications. LSU nrDNA million generations with sampling every 1000 genera­ sequences of the field-collected plants and cultures tions. A burn in sample of 2000 trees was removed were identical. before constructing the majority rule consensus tree. Field collected plants from Mexico have a typical C. a n te n n in morphology a (Figs 2-5), forming erect brush­ like tufts, 1—5(—8) cm high, composed of straight, rigid RESULTS filaments. Plants are firmly attached to the substrate by The Bl tree (Fig. 1) placed all Chaetomorpha antennina rhizoids sprouting from the proximal pole of the basal specimens in a clade of closely related sequences, cells, forming a compact basal mat. The elongated, © 2011 Japanese Society of Phycology Atypical development of Chaetomorpha 93 formed unilaterally (Figs 9,13) or in pairs along the stoloniferous rhizoids (Figs 10,12 and 19). The upright cells divide repeatedly by intercalary cell divi­ sion (centripetal invagination of the cell wall), result­ ing in unbranched, septate filaments (Figs 20,34). Cells of the upright filaments are cylindrical, 150- 250 pm in diameter and 300-900 pm long. The basal cells of the filaments are up to 3.5 mm long and lack annular constrictions. In numerous fila­ ments, cells produce
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