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Comparative Study
. 2005 Aug;170(4):1601-10.
doi: 10.1534/genetics.105.044503. Epub 2005 Jun 14.

Portrait of a species: Chlamydomonas reinhardtii

Thomas Pröschold  1 , Elizabeth H Harris, Annette W Coleman
Affiliations
Comparative Study

Portrait of a species: Chlamydomonas reinhardtii

Thomas Pröschold et al. Genetics. 2005 Aug.

Abstract

Chlamydomonas reinhardtii, the first alga subject to a genome project, has been the object of numerous morphological, physiological, and genetic studies. The organism has two genetically determined mating types (plus and minus) and all stages of the simple life cycle can be evoked in culture. In the nearly 60 years since the first standard laboratory strains were isolated, numerous crosses and exchanges among laboratories have led to some confusion concerning strain genealogy. Here we use analyses of the nuclear internal transcribed spacer regions and other genetic traits to resolve these issues, correctly identify strains currently available, and analyze phylogenetic relationships with all other available similar chlamydomonad types. The presence of a 10-bp indel in ITS2 in some but not all copies of the nuclear ribosomal cistrons of an individual organism, and the changing ratios of these in crosses, provide a tool to investigate mechanisms of concerted evolution. The standard C. reinhardtii strains, plus C. smithii +, plus the new eastern North American C. reinhardtii isolates, comprise one morphological species, one biological species of high sexual intercompatibility, and essentially identical ITS sequences (except the tip of helix I of ITS2). However, variant RFLP patterns characterize strains from each geographic site.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
Alignment of ITS2, hairpin loop I, sequences of standard C. reinhardtii “short” and “long,” plus that of C. smithii + and of the closely related Chlamydomonas strains. Paired nucleotide positions in standard C. reinhardtii are overlain with a line. An X marks the nucleotide diagnostic for standard C. reinhardtii vs. C. smithii +. The strains CC-1952, CC-2342, CC-2931, and CC-2935 are newly collected (sources given) and interfertile with standard C. reinhardtii. No long variant was obtained among the few subclones of CC-2931 sequenced. At the bottom are listed the five special primers used (paired with Grev) for analysis of the ITS2 helix I indel.
F<sc>igure</sc> 2.—
Figure 2.—
Secondary-structure diagram of Chlamydomonas reinhardtii ITS2 RNA transcripts. In the ITS2 diagram, the relatively conserved positions (Mai and Coleman 1997) are presented in boldface type. All nucleotide variants of the standard C. reinhardtii and of C. smithii + are indicated by arrows. (A) ITS1. Four nucleotide variants were each found in only one subcloned sequence of the standard C. reinhardtii strains (in order, CC-278, CC124J, CC-620, and UTEX 2247); the nucleotide in parentheses was a variant in one subclone of C. smithii +. (B) ITS2 had no variant nucleotide positions among all the standard C. reinhardtii subclones sequenced; as indicated by the arrows, in C smithii +, one subclone had a variant position, compensatory for pairing, in helix II, while all C. smithii + differed from all standard C. reinhardtii at the circled position in helix I. Shown in addition to the “long” form of helix I is the alternative “short” form of helix I, found in differing proportions in the standard C. reinhardtii strains. In the short form, the AflIII site is highlighted in boldface type. Only the short form, with the C substitution, has been recovered so far from C. smithii +, which is otherwise identical to C. reinhardtii in both ITS1 and ITS2.
F<sc>igure</sc> 3.—
Figure 3.—
Genealogy of standard C. reinhardtii laboratory strains, modified from Harris (1989). Note that CC-1690 (thick box) was used for creation of EST libraries for cDNA sequencing in the Chlamydomonas Genome Project. The three major sublines each are uniform for the genetic loci cited, with certain striking exceptions. In subline 1, two strains that Sager had by 1980 (UTEX 2246 and 2247) are unlike the remainder of subline 1 and probably came from the Gillham laboratory in an exchange. In subline 3, the CC-124J in Matsuda's laboratory, although obtained from Harris in 1983, is almost pure for the “long” ITS2 form, in contrast with the other subline 3 strains. Likewise, all the strains derived from the cell-wall-less mutants of Davies and Plaskitt (1971) are almost pure “shorts,” while the remainder of subline 3 are clearly mixed for ITS2 type. Data for mmp1-mmp2 are from Kubo et al. (2002). In sublines I and II, the + mating type has the RFLP allele called A for the mmp1-mmp2 region of linkage group XIX, while the − mating type has the B allele. In subline III, both mating types carry the A allele. The final metalloprotease gene (mmp3) is not yet mapped but segregates independently of all the other loci and also has two alleles by RFLP analysis. Again, in lines I and II, the + mating types have the A allele and the − mating type the B, while in subline III both mating types carry the A allele for this gene.
F<sc>igure</sc> 4.—
Figure 4.—
Possible origin of standard Chlamydomonas reinhardtii strains. The distribution of alleles in sublines I, II, and III cannot be accommodated in a single tetrad, but could be generated if at least one F1 is included.
F<sc>igure</sc> 5.—
Figure 5.—
Phylogenetic analyses of Chlamydomonas reinhardtii strains and putative relatives. (A) Tree, based on comparisons of the relatively conserved positions of ITS-2 of 36 taxa (116 positions marked in boldface type in Figure 2B), representing a maximum-likelihood analysis using the model according to Tamura and Nei (1993) with equal base frequencies and Gamma distribution shape parameter (G = 0.3853; TrNef + G). The model was calculated as the best model with Modeltest 3.06 (Posada and Crandall, 1998). The upper bootstrap values are neighbor joining (boldface type; 1000 replicates), using the same model criteria; the lower bootstrap values are maximum parsimony (boldface italic type; 1000 replicates). The tree was rooted using the basal clade, marked with a bracket. (B) The smaller tree presents the further analysis of the 23 nearest neighbors of C. reinhardtii (boxed in A, a branch marked with an asterisk), using the entire ITS-1 and ITS-2 sequence (851 positions) and strains UTEX 1341 and SAG 73.81 as outgroup. The tree was obtained using maximum-likelihood analysis, the Tamura and Nei model (TrN + I + G), with the proportion of invariable sites (I = 0.2182) and Gamma distribution shape parameter (G = 0.5983) calculated as best model with Modeltest. The bootstrap values are neighbor joining (boldface type; 1000 replicates), using the same model above and maximum parsimony (boldface italic type; 1000 replicates) below. Only bootstrap values >50% are presented. Taxon names in boldface type are newly sequenced here. The brace on the tree in B indicates interfertile Chlamydomonas strains.
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References

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