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Reconstructing the Basal Angiosperm Phylogeny: Evaluating Information Content of Mitochondrial Genes

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Reconstructing the Basal Angiosperm Phylogeny: Evaluating Information Content of Mitochondrial Genes 55 (4) • November 2006: 837–856 Qiu & al. • Basal angiosperm phylogeny Reconstructing the basal angiosperm phylogeny: evaluating information content of mitochondrial genes Yin-Long Qiu1, Libo Li, Tory A. Hendry, Ruiqi Li, David W. Taylor, Michael J. Issa, Alexander J. Ronen, Mona L. Vekaria & Adam M. White 1Department of Ecology & Evolutionary Biology, The University Herbarium, University of Michigan, Ann Arbor, Michigan 48109-1048, U.S.A. [email protected] (author for correspondence). Three mitochondrial (atp1, matR, nad5), four chloroplast (atpB, matK, rbcL, rpoC2), and one nuclear (18S) genes from 162 seed plants, representing all major lineages of gymnosperms and angiosperms, were analyzed together in a supermatrix or in various partitions using likelihood and parsimony methods. The results show that Amborella + Nymphaeales together constitute the first diverging lineage of angiosperms, and that the topology of Amborella alone being sister to all other angiosperms likely represents a local long branch attrac- tion artifact. The monophyly of magnoliids, as well as sister relationships between Magnoliales and Laurales, and between Canellales and Piperales, are all strongly supported. The sister relationship to eudicots of Ceratophyllum is not strongly supported by this study; instead a placement of the genus with Chloranthaceae receives moderate support in the mitochondrial gene analyses. Relationships among magnoliids, monocots, and eudicots remain unresolved. Direct comparisons of analytic results from several data partitions with or without RNA editing sites show that in multigene analyses, RNA editing has no effect on well supported rela- tionships, but minor effect on weakly supported ones. Finally, comparisons of results from separate analyses of mitochondrial and chloroplast genes demonstrate that mitochondrial genes, with overall slower rates of sub- stitution than chloroplast genes, are informative phylogenetic markers, and are particularly suitable for resolv- ing deep relationships. KEYWORDS: Amborella, basal angiosperms, magnoliids, mitochondrial genes, Nymphaeales, RNA editing. lowed by Austrobaileyales (Mathews & Donoghue, 1999, INTRODUCTION 2000; Parkinson & al., 1999; Qiu & al., 1999, 2000, 2001, The basal angiosperms have been subject to some of 2005; P. Soltis & al., 1999; Barkman & al., 2000; Graham the most intensive phylogenetic analyses ever conducted & Olmstead, 2000; D. Soltis & al., 2000; Zanis & al., on any group of organisms using numerous methods on a 2002; Borsch & al., 2003, 2005; Hilu & al., 2003; Aoki & large number of molecular markers over the last fifteen al., 2004; Kim & al., 2004; Stefanovic & al., 2004; years (Martin & Dowd, 1991; Hamby & Zimmer, 1992; Goremykin & al., 2005; Leebens-Mack & al., 2005; Chase & al., 1993; Qiu & al., 1993, 1999, 2000, 2001, Löhne & Borsch, 2005). The remaining angiosperms 2005; D. Soltis & al., 1997, 2000; Hoot & al., 1999; (euangiosperms, cf. Qiu & al., 1999) are divided into five Mathews & Donoghue, 1999, 2000; Parkinson & al., lineages: Chloranthaceae, Ceratophyllum, monocots, 1999; Renner, 1999; P. Soltis & al., 1999; Barkman & al., magnoliids, and eudicots (Qiu & al., 1999, 2000, 2005; 2000; Graham & Olmstead, 2000; Savolainen & al., 2000; Zanis & al., 2002; Hilu & al., 2003). There is no strongly Nickrent & al., 2002; Zanis & al., 2002, 2003; Borsch & supported, generally agreed resolution on relationships al., 2003; Goremykin & al., 2003, 2005; Hilu & al., 2003; among these five lineages, except that Ceratophyllum has Sauquet & al., 2003; Aoki & al., 2004; Kim & al., 2004; been accepted to be sister to eudicots by The Angiosperm Stefanovic & al., 2004; Leebens-Mack & al., 2005; Löhne Phylogeny Group (2003). The magnoliids are composed & Borsch, 2005). As a result, this abominably mysterious of four well-defined taxa, Magnoliales, Laurales, group of plants are among the best known for their long- Canellales, and Piperales, which form two pairs of sister thought unknowable evolutionary history among many groups. The monophyly of magnoliids and relationships similarly difficult groups of organisms on the tree of life. among the four member lineages have received steady At present, the following consensus is emerging. increase of bootstrap support as more data are added in Amborella or Amborella + Nymphaeales represent the the analysis (Mathews & Donoghue, 1999; Qiu & al., earliest-diverging lineage of extant angiosperms, fol- 1999, 2005; Zanis & al., 2002). 837 Qiu & al. • Basal angiosperm phylogeny 55 (4) • November 2006: 837–856 Exploration in several dimensions have been pursued tion rates can yield less homoplasious characters and in this exemplar case of phylogenetic reconstruction. intron presence/absence can be used as informative char- Increasing taxon sampling represents one of the earliest acters), while others may not be as problematic as previ- and main assaults on this long-standing problem (Chase ously thought, such as the lineage-specific rate hetero- & al., 1993; D. Soltis & al., 1997, 2000; Savolainen & al., geneity, horizontal gene transfer, and RNA editing, as 2000; Hilu & al., 2003). Selection of markers from dif- long as the care is taken to deal with these problems. A ferent genomes, encoding different functions, and evolv- large number of studies that have employed mitochondri- ing at different rates was also attempted right from the al genes and introns for phylogenetic reconstruction beginning and received a major boost after automated across land plants support this evaluation (Hiesel & al., sequencing became available (Martin & Dowd, 1991; 1994; Malek & al., 1996; J. Davis & al., 1998, 2004; Qiu Hamby & Zimmer, 1992; Qiu & al., 1993, 1999, 2005; D. & al., 1998, 1999, 2005, in press; Beckert & al., 1999, Soltis & al., 1997; Mathews & Donoghue, 1999; Graham 2001; Duff & Nickrent, 1999; Vangerow & al., 1999; & Olmstead, 2000; Savolainen & al., 2000; Borsch & al., Barkman & al., 2000, 2004; Bowe & al., 2000; Chaw & 2003, 2005; Hilu & al., 2003; Aoki & al., 2004; Kim & al., 2000; Wang & al., 2000; Gugerli & al., 2001; al., 2004; Löhne & Borsch, 2005). Relative merits of Anderberg & al., 2002; Nickrent & al., 2002; Sanjur & character versus taxon sampling on influencing tree al., 2002; Cox & al., 2004; Dombrovska & Qiu, 2004; topology stability have been investigated in several recent Qiu & Palmer, 2004; Groth-Malonek & al., 2005; Guo & studies (Graham & Olmstead, 2000; Goremykin & al., Ge, 2005; Wikström & Pryer, 2005). At a time when 2003, 2005; Stefanovic & al., 2004, Leebens-Mack & al., many problems in the angiosperm and land plant phylo- 2005). Finally, experimentation with different methods of genies are still unresolved and suitable markers from the data analysis (e.g., constraint analysis/alternative topolo- nuclear genome that can be used on wide taxonomic gy testing, noise reduction, compartmentalization, and scales without the problem of paralogy are limited in synapomorphic sites identification) and rooting tech- number, the mitochondrial genome remains the only other niques (e.g., duplicated gene rooting and random viable choice and a fertile ground for exploration outside sequence outgroup rooting), besides regular application the chloroplast genome. Furthermore, for many deep rela- of parsimony, likelihood, and distance methods as well as tionships in the angiosperm and land plant phylogenies, bootstrapping, jackknifing, and decay analyses, have because of their controversial nature and volatility, it is been performed to specifically address the rooting issue imperative to use information from a different genome to and robustness of parts of the internal topology (Qiu & evaluate independently the results that are derived largely al., 1993, 2000, 2001, 2005; Mathews & Donoghue, from chloroplast genes (Qiu & Palmer, 1999). Therefore, 1999; Parkinson & al., 1999; Barkman & al., 2000; Zanis the potential for mining historical signals from the mito- & al., 2002, 2003). These efforts have undoubtedly con- chondrial genome to understand the evolutionary history tributed to the progress on our understanding of relation- of plants deserves a serious and careful assessment. ships among basal angiosperms. To solve remaining prob- In this study, we analyze eight mitochondrial, chloro- lems, more data sources and analytic methods need to be plast, and nuclear genes from all major lineages of gym- explored. nosperms and angiosperms using both maximum likeli- Among three genomes within the plant cell, the mito- hood and maximum parsimony methods, aiming to chondrial genome was the last to be utilized for phyloge- achieve two goals. We first want to use these data (1) to netic reconstruction. This situation might have been determine whether the earliest-diverging lineages of caused by the perception that several features of mito- extant angiosperms consists of Amborella alone or chondrial genes were undesirable. These include low sub- Amborella + Nymphaeales, (2) to evaluate the monophy- stitution rates, the dramatic lineage-specific rate hetero- ly of magnoliids and sister relationships between geneity, abundant occurrence of introns (many of which Magnoliales and Laurales, and between Canellales and are trans-spliced, making PCR difficult), idiosyncratic Piperales, and (3) to resolve relationships among RNA editing patterns across genes and lineages, some- Chloranthaceae, Ceratophyllum, magnoliids, monocots, times frequent losses from the genome, and horizontal and eudicots. We then want to use this case of recon- transfers
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