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Four Embryophyte Introns and Psbb Operon Indicate Chlorokybus As a Basal Streptophyte Lineage

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Four Embryophyte Introns and Psbb Operon Indicate Chlorokybus As a Basal Streptophyte Lineage Algae Volume 17(1): 53-58, 2002 Four Embryophyte Introns and psbB Operon Indicate Chlorokybus as a Basal Streptophyte Lineage Jungho Lee1,2,* and James R. Manhart2 1Institute of Systematic Botany, University of Zürich, Zollikerstrasse 107, 8008 Zürich, Switzerland and 2Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA. The transition of plant life from aquatic algae to land plants was one of the major events in the history of life. However, in hypothesizing the exact evolutionary path of the transition, limited shared phenotypic characters in aquatic algae and land plants (embryophytes) have been a major hinderance. Chloroplast genomes contain charac- ters useful in tracing evolutionary histories. Embryophyte chloroplast genomes are distinguished from algal cpDNAs by having over 20 group II introns, some of which were gained during the transition from algae to embryophytes (Manhart and Palmer 1990; Lew and Manhart 1993; Lee and Manhart 2002). Here we examine a gene cluster that, in land plants, contains psbB, psbT, psbH, petB and petD with introns found in petB and petD (petB.i and petD.i). In addition the presence/absence of introns in trnA and trnI (trnA.i and trnI.i) were determined in all five major lineages of charophytes. We found that the psbB gene cluster occurs in most surveyed charophytes and embryophytes except Spirogyra (Zygnematales) which lacks it due to intra-genomic rearrangement. All four introns are absent in Chlorokybus but present in some or all of the other four charophyte lineages (Klebsormidiales, Zygnematales, Coleochaetales, and Charales). In addition, Chlorokybus is distinguished from other charophytes and embryophytes by having an unusually long spacer (over 2 kb) between psbH-petB. The results indicate that Chlorokybus diverged before the intron gains but after psbB gene cluster formation, placing the other charophyte lin- eages closer to embryophytes. Key Words: charophytes, Chlorokybus, group II intron, petB, petD, psbB operon, streptophytes, trnA, trnI cate the split of Chlorokybales and other streptophytes INTRODUCTION (Bremer 1985; Mishler and Churchill 1985). Another cladistic study of non-molecular data actually placed Chlorokybus atmophyticus Geitler, the sole species in the Zygnematales as the first branch of streptophytes Chlorokybales (Mattox and Stewart 1983), was recog- (Sluiman 1985). Phylogenetic analyses of nuclear 18S nized as a charophyte only twenty years ago when it rDNA sequences, on the other hand, have placed either was shown to possess a multilayered structure (MLS) – a Chlorokybales (Wilcox et al. 1993; Bhattacharya and unique organization of cytoskeletal microtubules in the Medlin 1998), Charales (Kranz et al. 1995) or a clade of swimming sperms of streptophytes, and zoospores simi- Chlorokybales-Klebsormidiales-Zygnematales- lar to charophytes (Rogers et al. 1980). Several other fea- Coleochaetales at the base of streptophytes (Melkonian tures were identified later to strengthen this relationship: et al. 1995). Recent analysis of 18S rDNA, actin gene open spindles, motile cells lacking eyespots and rhizo- sequences, and four gene analyses have also shown that plasts, and right-oriented flagella (Bremer 1985; Mishler Mesostigma viride, previously classified as a member of and Churchill 1985). From the beginning, it was suggest- the Prasinophyceae, is sister to streptophytes (Melkonian ed that Chlorokybus may represent the most primitive et al. 1995; Bhattacharya et al. 1998; Karol et al. 2001). charophyte based on its zoospore release mechanism, Nevertheless, it remains to be seen whether this alga sarcinoid growth and retention of scaly covering (Rogers possesses all of the features that define streptophytes. et al. 1980). Rigorous cladistic analyses, however, uncov- Given our understanding now that reconstruction of ered only one character, filamentous growth, to demar- ancient evolutionary histories requires extensive sam- pling of both taxa and characters (Qiu and Palmer 1999; *Corresponding author ([email protected] or Qiu and Lee 2000), some of the results from these molec- [email protected]) 54 Algae Vol. 17(1), 2002 ular analyses are probably artefacts due to sampling (Invitrogen) for sequencing (detailed primer information errors and/or remote outgroup. We took an approach of is available from JL; see also Lee and Manhart 2002). searching for infrequent genomic structural changes, Sequencing was done on an ABI-PRISM 377 DNA such as intron gains and operon formation, which have sequencer (PE Applied Biosystems). Sequence analysis been used successfully to resolve ancient diversification was carried out using GCG package (Genetics Computer patterns (Manhart and Palmer 1990; Baldauf et al. 1990; Group, Inc.). Complete gene cluster sequences are Qiu et al. 1998) to determine relationships of chloro- deposited in GenBank under accession numbers phytes and streptophytes. AF482495-AF482503. MATERIALS AND METHODS RESULTS AND DISCUSSION Micro-algal strains from ACOI (Univerdidade de The four group II introns, one each from the genes Coimbra, Portugal), SAG (Sammlung von petB (petB.i), petD (petD.i), trnA (trnA.i), and trnI (trnI.i), Algenkulturen, University of Gottingen, Germany), and are known to be widespread in land plants (Ohyama et UTEX (University of Texas, Austin) were used in this al. 1986; Shinozaki et al. 1986; Hiratsuga et al. 1989; Wolfe study. Macro-algae were collected from the wild (vouch- et al. 1992; Wakasugi et al. 1994; Sato et al. 1999; Kato et al. ers and the herbaria at Texas A&M University (TAMU) 2000; Hupfer et al. 2000; Schmitz-Linneweber et al. 2001). and University of Zürich (Z). Micro-algal cultures Two of them, trnA.i and trnI.i, have also been found in a include Chlorokybus atmosphyticus (UTEX LB 2591), few charophytes (Manhart and Palmer 1990). On the Klebsormidium bilatum (SAG 31.91), Kelsormidium nitens other hand, completely sequenced chloroplast genomes (SAG B 5.96), Closterium acerosum (UTEX LB 1075), from eight non-charophyte algae, which spans the full Cosmarium botrytis (UTEX 301), Staurastrium pinge (UTEX diversity of photosynthetic eukaryotes, show the LB1606), Spirogyra maxima (UTEX LB 2495 (see Manhart absence of these introns (Kowallick et al. 1995; Stirewalt et al. 1990, Manhart and Palmer 1990), Sirogonium et al. 1995; Reith and Munholland 1995; Wakasugi et al. melanosporum (Hoshaw culture-716, see Hoshaw 1980, 1997; Turmel et al. 1999; Douglas and Penny 1999; Baldauf et al. 1990 and Manhart 1994), Coleochaete orbicu- Lemieux et al. 2000; Glockner et al. 2000). PCR was used laris (UTEX LB 2651, see Manhart and Palmer 1990 and to amplify the intron-containing portion of the genes Baldauf et al. 1990), and Chaetosphaeridium pringsheimii from total cellular DNAs. In the cases of Chara fibrosa, (ACOI 737). Macro-algae are Chara fibrosa (Manhart, Coleochaete orbicularis, Spirogyra maxima, chloroplast Texas A&M Field Station, College Station, TX, US; genomic clones that contain the genes were sequenced. TAMU), Chara vularis (Lee 7001-1996, Bull Creek, Austin, A total of 13 species, from 11 genera of all five orders of TX, US; TAMU), Nitella mucronata (Preisig et al. 1998, charophytes (Mattox and Stewart 1983) were investigat- Zurich Botanical Garden culture, Switzerland; Z), ed. The introns petB.i and trnA.i are present in all or Nitellopsis obtusa (Buzgo et al. 1998, male plant, Zurich some species of Charales, Coleochaetales, Zygnematales lake, Switzerland; Z). and Klebsormidiales, but not in Chlorokybus (Fig. 1). The Chloroplast DNAs of Chara fibrosa, Coleochaete intron trnI.i is present in all examined species of orbicuaris and Spirogyra maxima were isolated as Charales, Coleochaetales and Klebsormidiales, but not in described in Baldauf et al. (1990) and shotgun cloned as some species of Zygnematales or Chlorokybus. The most described in Manhart et al. (1990) and Lee and Manhart variable distribution pattern was observed for petD.i, (2002). For other taxa, PCR from total cellular DNAs which is present in both genera of Coleochaetales and were used. Total cellular DNA was isolated using the only some species of Charales and Zygnematales but standard CTAB method and purified either by CsCl den- absent entirely in Klebsormidiales and Chlorokybus. sity gradient ultracentrifugation (Baldauf et al. 1990). The Presence or absence of these introns was verified by gene or gene cluster was located by end-sequencing of sequencing the PCR products. In all cases, the introns clones and sub-clones in three taxa as described in Lee were found to be located at precisely the same positions and Manhart (2002). The genes (and introns) of other as those in land plants (Fig. 2). Their sequence identities than genomic cloned taxa were amplified using the con- to their counterparts in Marchantia range from 52-74% ventional PCR method. PCR products were either direct- (only for alignable stretches of sequences), and the ly sequenced or cloned using TOPOTM TA Cloning kit introns in Marchantia are 63-78% identical to those in Lee & Manhart: Embryophyte Introns and psbB Operon 55 Fig. 1. Distribution of four chloroplast introns in land plants, charophytes and non-charophyte algae. Open squares indicate intron absence. Filled squares indicate intron pres- ence. Intron data are obtained from diagnostic PCR, sequencing, or both. Klebsormidium species are 1 - K. nitens and 2 - K. bilatum. Chara species are 1 - C. vulgaris and 2 - C. fibrosa. NCH - non-chlorophytes, CHL - Chlorophyta sensu stricto, BST - basal streptophytes,
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