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As the Primal Extant Monocotyledon (Molecular Systematics/Phylogenetics/Ribulose-Bisphosphate Carboxylase) MELVIN R

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As the Primal Extant Monocotyledon (Molecular Systematics/Phylogenetics/Ribulose-Bisphosphate Carboxylase) MELVIN R Proc. Natl. Acad. Sci. USA Vol. 90, pp. 4641-4644, May 1993 Evolution Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon (molecular systematics/phylogenetics/ribulose-bisphosphate carboxylase) MELVIN R. DUVALL*, GERALD H. LEARN, JR., Luis E. EGUIARTEt, AND MICHAEL T. CLEGG Department of Botany and Plant Sciences, University of California, Riverside, CA 92521-0124 Contributed by Michael T. Clegg, March 12, 1993 ABSTRACT The identity of the oldest lineage of monocot- across the monocotyledons from 116 species, which sug- yledons is a subject of debate. Alternative interpretations of gested a phylogenetic framework for the entire group (7). morphological homologies are variously consistent with pro- Here we present an exhaustive analysis of molecular evi- posals that species of Aflsmatanae, Dioscoreales, or Melanthi- dence from selected representatives in all major groups (all ales were the earliest descendants of the first monocotyledons. superorders excluding Triuridanae; see explanation below) to We present phylogenetic analyses based on DNA sequences of identify the primal extant lineage and to outline higher-order the plastid locus rbcL in which Acorus calamus, an herb with relationships. unspecialized floral features and of uncertain affmities, is One species in this study, Acorus calamus, or sweet flag, supported as a member of the oldest extant lineage of mono- deserves particular comment. Systematists have sought to cotyledons. This condusion is consistent with a substantial establish the affinities of Acorus, which exhibits a unique body of morphological, anatomical, and embryological evi- combination of characteristics. Two of the most remarkable dence and offers an explanation for the failure to identify any of these are (i) a cellular type of endosperm development close relationship between Acorus and other genera. which is otherwise unknown in monocotyledons but common in dicotyledons (9) and (ii) a reported absence of double Primal monocotyledons are thought to have diverged from fertilization, unlike virtually all angiosperms (10). The flow- dicotyledons 100-150 million years ago by one of several ers of Acorus, which are bisexual, perigoniate, and trimer- proposed evolutionary scenarios (1). Proponents of the once ous, resemble those of primitive Aranae, the sister super- widely accepted "phyllode theory" held that the nature of order to the Alismatanae, but also those of primitive mono- the typically linear monocotyledonous leaf indicated homol- cotyledons in general. Nonetheless, these characteristics, ogy to an elaborated dicotyledonous petiole (ref. 2; but see together with a superficial resemblance in leafmorphology to refs. 3 and 4 for countering arguments). This presumed the Australian aroid Gymnostachys anceps have been used to homology supported an ancestry from aquatic dicotyledons justify the traditional classification ofAcorus in Aranae (1, 2, with reduced leaves, leading to the conclusion that the most 5, 11, 12). ancient monocotyledons were to be found among aquatic Extensive investigations of the numerous unique embryo- Alismatanae (water plantains and allied species). Alterna- logical, anatomical, and floral characteristics ofAcorus argue tively, supporters of what has been designated, somewhat against a close relationship with Aranae (9, 13-16). However, loosely, as the "magnolianan hypothesis" (so-called because no other group of monocotyledons displays more convincing of a presumed ancestry from pre-Magnolianae) propose that evidence of alliance. The only proposed alternative candi- the atypical, petiolate, reticulately veined leaves of dios- dates are species of Typhales with which Acorus shares coreoid monocotyledons (yams and related species) are ho- several similarities of anatomy, morphology, and embryol- mologous to those ofdicotyledons (1). This scenario suggests ogy (9) and a host relationship with the same fungal parasite that the primal monocotyledons, presumably now extinct, (17). Because of its extraordinary features and problematic first gave rise to the ancestors of Lilianae rather than of systematic history Acorus calamus was included in our Alismatanae. Other lineages, including the melanthioid lilies, analysis, together with putatively related species (Aranae, 10 have also been proposed to be primal (5). Since the mono- species; Typhales, 2 species). cotyledons are believed to share a single common ancestry The plastid locus rbcL encodes the large subunit of ribu- (1, 6-8), only one ofthese hypotheses can be correct. Clearly lose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). there is no consensus on which lineages of monocotyledons RuBisCO, the most abundant soluble leaf protein, is an are distinguished as the most ancient, nor are the relation- indispensable component of photosynthetic carbon metabo- ships among the major groups well resolved. Morphological lism and is thus ubiquitous among green plants. (Note that homologies are too ambiguous to decide among the compet- one superorder of monocotyledons, Triuridanae, is com- ing hypotheses. Until these issues are clarified, the origin and posed exclusively of nonphotosynthetic species that are subsequent evolutionary history that produced the 50,000 unlikely to possess a functional, and therefore phylogeneti- species of monocotyledons will remain an enigma. cally meaningful, copy of the rbcL sequence.) Furthermore, The failure to resolve the higher-order taxonomic relation- because the locus is highly conserved and lacks introns, the ships among monocotyledons is due to an inability to identify alignment of sequences ofrbcL from long-diverged species is evolutionarily meaningful homologies between long-diverged a straightforward matter. Finally, the utility of rbcL data for species. Analysis ofmolecular characters has the potential to phylogenetic reconstructions has been amply demonstrated circumvent this difficulty. However, the only inclusive in- (6-8, 18-23). vestigation of the molecular systematics of monocotyledons is our broad analysis of plastid DNA sequences sampled Abbreviation: MLE, maximum likelihood estimation. *Present address: Nucleic Acid Facility, 1184 Molecular Biology Building, Iowa State University, Ames, IA 50011-3260. The publication costs ofthis article were defrayed in part by page charge tPresent address: Centro de Ecologia, Universidad Nacional Au- payment. This article must therefore be hereby marked "advertisement" tonoma de Mexico, Apdo. Postal 70-275, 04510 Mexico, D.F., in accordance with 18 U.S.C. §1734 solely to indicate this fact. Mexico. 4641 Downloaded by guest on September 27, 2021 4642 Evolution: Duvall et al. Proc. Natl. Acad. Sci. USA 90 (1993) MATERIALS AND METHODS RESULTS AND DISCUSSION DNA sequences of a 1327-base-pair portion of the rbcL gene For the 27 monocotyledonous species, ofthe 1320 nucleotide were determined for 10 species: Anchomanes difformis, sites analyzed, 437 (33%) were polymorphic, with 71, 49, and Ariopsis peltata, Lasia spinosa, Montrichardia arborescens, 317 polymorphisms observed atfirst, second, and third codon Symplocarpus foetidus, Xanthosoma sagittifolium positions, respectively. (Araceae), Eriocaulon microcephalum (Eriocaulaceae), The tree with the largest log-likelihood score (-8733.036) Hosta rectifolia (Funkiaceae), Ludovia integrifolia (Cyclan- from the MLE analysis is given (Fig. 1). Tests (30) of the thaceae), and Orthrosanthus polystachyus (Iridaceae). Total log-likelihood scores of all topologies produced by the MLE genomic DNA was isolated from dried shoots (24) of Erio- method indicated no significant differences in scores. A strict caulon microcephalum and from fresh leaves (35) ofthe other consensus ofthese trees is given (Fig. 2). Parsimony analysis 9 species. Approximately 1 jig of each DNA preparation was produced 40 equally parsimonious trees of length 1237 (re- used to provide template for Taq-mediated amplification of tention index = 0.547), the strict consensus ofwhich is given the rbcL gene using the protocol provided with Taq DNA together with bootstrap values (Fig. 3). The single difference polymerase by the supplier (Promega) and synthetic primers between the resolved portions of the two consensus trees homologous to between Zea (Figs. 2 and 3) is the position of Sagittaria graminea (Alis- conserved regions mays and matanae), which is embedded in Aranae in the parsimony Spinacia oleracea. The forward primer is homologous to the analysis (Fig. 3). The phylogenetic position ofthis species in first 27 base pairs ofrbcL and the reverse primer corresponds the parsimony analysis is clearly an artifact of sampling too to positions 1355-1378 on the complementary strand. Single- few taxa, as was shown by analyses including rbcL data from stranded DNA for direct sequencing was prepared in subse- other species of Alismatanae (not shown). quent amplifications. Primers for sequencing were designed In the optimized topologies produced by both maximum- and made available by G. Zurawski (DNAX, Palo Alto, CA) likelihood and parsimony methods there is a basal split based on oligonucleotide sequences conserved between the between A. calamus and the remaining 26 monocotyledons, rbcL sequences ofZea mays and Spinacia oleracea. By these methods, 1327 base pairs of rbcL were determined for 10 - ~Bambusa species representing four superorders of monocotyledons. Joinvillea The rbcL sequences for these 10 species have been deposited Cyperus in the GenBank data base under accession numbers L10246- L10255.
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