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Complex Patterns of Plastid 16S Rrna Gene Evolution in Nonphotosynthetic Green Algae

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Complex Patterns of Plastid 16S Rrna Gene Evolution in Nonphotosynthetic Green Algae J Mol Evol (2001) 53:670–679 DOI: 10.1007/s002390010254 © Springer-Verlag New York Inc. 2001 Complex Patterns of Plastid 16S rRNA Gene Evolution in Nonphotosynthetic Green Algae Aurora M. Nedelcu Department of Ecology and Evolutionary Biology, Biological Sciences West Building, Room 310, University of Arizona, Tucson, AZ 85721, USA Received: 29 December 2000 / Accepted: 18 May 2001 Abstract. This study provides a phylogenetic/ Key words: 16S rRNA — Plastid — Nonphotosyn- comparative approach to deciphering the processes un- thetic — Insertion — Repair — Polytoma — Prototheca derlying the evolution of plastid rRNA genes in genomes under relaxed functional constraints. Nonphotosynthetic green algal taxa that belong to two distinct classes, Chlo- rophyceae (Polytoma) and Trebouxiophyceae (Proto- Introduction theca), were investigated. Similar to the situation de- scribed previously for plastid 16S rRNA genes in nonphotosynthetic land plants, nucleotide substitution Evolution is often associated with loss of functions and/ levels, extent of structural variations, and percentage AT or structures. One of the most dramatic evolutionary values are increased in nonphotosynthetic green algae losses is the loss of photosynthesis in green plants. Al- compared to their closest photosynthetic relatives. How- though “green” lineages are usually defined by their abil- ever, the mutational processes appear to be different in ity to photosynthesize, many nonphotosynthetic “green many respects. First, with the increase in AT content, plants,” both land plants and green algae, are known. more transversions are noted in Polytoma and holopara- Among such lineages are the parasitic nonphotosynthetic site angiosperms, while more transitions characterize the (holoparasitic) angiosperms (e.g., Scrophulariaceae/ evolution of the 16S rDNA sequences in Prototheca. Orobanchaceae) and the strictly heterotrophic (“color- Second, although structural variations do accumulate in less”) unicellular green algae (e.g., Polytoma, Polyto- both Polytoma and Prototheca (as well as holoparasitic mella, Prototheca). In both land plants and green algae, plastid 16S rRNAs), insertions as large as 1.6 kb char- loss of photosynthesis has occurred more than once: at acterize the plastid 16S rRNA genes in the former, least five times in Scrophulariales (dePamphilis et al. whereas significantly smaller indels (not exceeding 24 1997), at least four times among nonasterid plants (Nick- bp) seem to be more prevalent in the latter group. The rent et al. 1998), and at least four times in green algae differences in evolutionary rates and patterns within and (Rumpf et al. 1996; Huss et al. 1999). between lineages might be due to mutations in replica- The nonphotosynthetic land plants and green algae tion/repair-related genes; slipped-strand mispairing is investigated to date have been found to contain degen- likely the mechanism responsible for the expansion of erate plastids (leucoplasts) and/or plastid DNA (e.g., de- insertions in Polytoma plastid 16S rRNA genes. Pamphilis and Palmer 1990; Machado and Zetsche 1990; Haberhausen et al. 1992; Vernon 1996; Nickrent et al. 1997b). Leucoplast genomes in nonphotosynthetic plants are reduced in size and number of genes compared with Correspondence to: Aurora M. Nedelcu; e-mail: [email protected]. their counterparts in photosynthetic relatives (e.g., Mor- edu den et al. 1991; Wolfe et al. 1992a; Nickrent et al. 1997b). 671 The retention of a degenerate but potentially active Although information on plastid genes in nonphoto- plastid genome in all secondarily nonphotosynthetic synthetic plants is currently accumulating (e.g., Wolfe green plants is attributed to the presence of unidentified and dePamphilis 1997, 1998; dePamphilis et al. 1997; plastid genes whose protein products are thought to be Young et al. 1999), the forces and the mechanisms in- indispensable for the well-being of the organism (e.g., volved in the evolution of leucoplast genes are not fully Wolfe and dePamphilis 1998). It thus follows that the understood. The questions addressed in this study gene expression machinery is still present and may be include (i) What are the patterns and trends that charac- active in these degenerate plastids. Genes coding for terize the evolution of plastid 16S rRNA genes in non- components of the leucoplast transcriptional/translation- photosynthetic green algal lineages? (ii) Are these evo- al apparatus (e.g., rRNAs, tRNAs, elongation factors, lutionary patterns and trends similar or different among ribosomal proteins) indeed have been found in many heterotrophic green algal groups and between green al- holoparasitic plants (e.g., dePamphilis and Palmer 1990; gae and parasitic angiosperms? and (iii) Which are the Wimpee et al. 1991; Wolfe et al. 1992a; Nickrent et al. potential evolutionary forces and mechanisms underly- 1997a; Lohan and Wolfe 1998) as well as nonphotosyn- ing the evolution of plastid genes in nonphotosynthetic thetic green algae (Vernon 1996; Vernon et al. in press). green algal lineages? Although there is evidence that plastid genes are tran- A comparative/phylogenetic approach can provide scribed in some parasitic plants (e.g., Ems et al. 1995; information on these evolutionary processes and help Nickrent et al. 1997a), the actual cellular localization as distinguish between general and lineage-specific phe- well as the functionality of their products awaits further nomena. It is in this light that in the present study non- investigations. In addition, the transcription of plastid photosynthetic green algal lineages from two green algal genes is dependent upon components of the cytosolic groups, Polytoma and Prototheca, have been investi- gated. The former belongs to the class Chlorophyceae, expression machinery (such as RNA polymerase), which whereas the latter is included in the Trebouxiophyceae substitute for the plastid-encoded counterparts whose (sensu Friedl 1995). Polytoma consists of Chlamydomo- coding regions became pseudogenes (Lusson et al. nas-like biflagellate algae that affiliate with at least two 1998). distinct chlamydomonadalean clades (Rumpf et al. Generally, it is believed that the plastid translational 1996), whereas Prototheca species are nonflagellate al- machinery in nonphotosynthetic plants is subjected to gae that are related to Chlorella species (Huss et al. less stringent selection because, subsequent to the loss of 1999). photosynthesis in these lineages, translation levels drop (e.g., Morden et al. 1991; Wolfe et al. 1992b; dePamphi- lis et al. 1997). Indeed, some leucoplast genes that fea- ture accelerated rates of DNA sequence evolution, have Materials and Methods undergone major structural changes and/or have become pseudogenes (e.g., Wolfe et al. 1992b, c; dePamphilis et The classification, species names, source, and strain numbers of the al. 1997; Nickrent et al. 1997a; Wolfe and dePamphilis taxa investigated, as well as the accession numbers of the sequences analyzed in this study, are summarized in Tables 1 and 2. Algal cultures 1998). However, a study on the evolution of the gene were grown in the media indicated in Table 1. Cultures were axenic and encoding the plastid ribosomal protein S2 (rps2)inthe checked for bacterial contamination before nucleic acid extraction. To- Scrophulariaceae/Orobanchaceae lineage (which con- tal DNA and RNA were extracted as described previously (Nedelcu et tains free-living and parasitic plants) revealed that not all al. 1996, 2000). Total DNA from P. oviforme and the rrn16 sequence of P. obtusum were kindly provided by Dawne Vernon and C. William holoparasites appear to have accelerated rates of rps2 Birky, Jr. PCR amplifications were performed using a Stratagene Ro- evolution; on the other hand, some hemiparasites (i.e., bocycler and Platinum Taq DNA Polymerase High-Fidelity, Elongase photosynthetic parasites) do show increased rates (de- Enzyme Mix, and SuperScript One-Step RT-PCR System (Life Tech- Pamphilis et al. 1997). In addition, different mechanisms nologies). PCR primer sequences and their positions relative to the seem to be independently acting in the Scrophulariaceae/ Escherichia coli counterpart are summarized in Table 3. Where more than one PCR product was obtained, the major bands were individually Orobanchaceae lineage: lessening of functional con- excised, and the DNA was extracted, purified, and reamplified. The straints might be responsible for the increased rate of PCR products were cleaned using a Qiagen Gel Extraction Kit and/or nonsynonymous substitutions, but variations in muta- PCR Purification Kit and sequenced on both strands using the auto- tional or repair mechanisms are likely responsible for the mated sequencing facilities at the Laboratory for Molecular Systemat- ics and Evolution, University of Arizona, Tucson (http://www.arl.arizona. observed differences in synonymous rates (dePamphilis edu/lmse/). Sequences were aligned using Clustal V, and the align- et al. 1997). Furthermore, the increased rate of nonsyn- ments were refined manually, based on conserved secondary structure onymous substitutions was shown to be lineage specific features. Phylogenetic analyses were performed using PAUP version (Nickrent et al. 1998). Lineage-specific processes may 4.0 (Swofford 1998); gaps and unalignable regions were manually also be responsible for differences in the retention of a excluded from the analyses using MacClade version 4.0 (Madison and Madison 2000). Bootstrap analyses (100 replications) were conducted photosynthetic
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