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Mitochondrial DNA Sequences Reveal the Photosynthetic Relatives of Rafflesia, the World’S Largest Flower

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Mitochondrial DNA Sequences Reveal the Photosynthetic Relatives of Rafflesia, the World’S Largest Flower Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world’s largest flower Todd J. Barkman*†, Seok-Hong Lim*, Kamarudin Mat Salleh‡, and Jamili Nais§ *Department of Biological Sciences, Western Michigan University, Kalamazoo, MI 49008; ‡School of Environmental and Natural Resources Science, Universiti Kebangsaan Malaysia, 43600 Bangi, Selangor, Malaysia; and §Sabah Parks, 88806 Kota Kinabalu, Sabah, Malaysia Edited by Jeffrey D. Palmer, Indiana University, Bloomington, IN, and approved November 7, 2003 (received for review September 1, 2003) All parasites are thought to have evolved from free-living ances- flies for pollination (14). As endophytes growing completely tors. However, the ancestral conditions facilitating the shift to embedded within their hosts, Rafflesia and its close parasitic parasitism are unclear, particularly in plants because the phyloge- relatives Rhizanthes and Sapria are hardly plant-like because they netic position of many parasites is unknown. This is especially true lack leaves, stems, and roots and emerge only for sexual repro- for Rafflesia, an endophytic holoparasite that produces the largest duction when they produce flowers (3). These Southeast Asian flowers in the world and has defied confident phylogenetic place- endemic holoparasites rely entirely on their host plants (exclu- ment since its discovery >180 years ago. Here we present results sively species of Tetrastigma in the grapevine family, Vitaceae) of a phylogenetic analysis of 95 species of seed plants designed to for all nutrients, including carbohydrates and water (13). Cir- infer the position of Rafflesia in an evolutionary context using the cumscriptions of Rafflesiaceae have varied to include, in the mitochondrial gene matR (1,806 aligned base pairs). Overall, the strict sense, only Rafflesia, Rhizanthes, and Sapria; however, in estimated phylogenetic tree is highly congruent with independent the broad sense, the family includes the divergent endophytic analyses and provides a strongly supported placement of Rafflesia holoparasites Apodanthes, Pilostyles, Cytinus, Bdallophyton, and with the order Malpighiales, which includes poinsettias, violets, Mitrastema as well (15, 16). Regardless of strict or broad and passionflowers. Furthermore, the phylogenetic placement of interpretations of the family, all of these divergent parasitic Mitrastema, another enigmatic, holoparasitic angiosperm with the plants remain unclassified within the recent ordinal treatment of order Ericales (which includes blueberries and persimmons), was angiosperms (11). Molecular phylogenetic placement of Raffle- obtained with these data. Although traditionally classified to- sia using plastid DNA sequences has not been achieved because gether, Rafflesia and Mitrastema are only distantly related, imply- Rafflesia seems to lack the commonly studied gene rbcL (4) and ing that their endoparasitic habits result from convergent evolu- may not have a plastid genome at all (7). Furthermore, molecular tion. Our results indicate that the previous significant difficulties studies of the nuclear 18S gene from Rafflesia indicate that it associated with phylogenetic placement of holoparasitic plants evolves at least 3.5 times faster than in photosynthetic plants may be overcome by using mitochondrial DNA so that a broader (17). This rate acceleration has frustrated previous attempts to EVOLUTION understanding of the origins and evolution of parasitism may infer its phylogenetic position (4, 18). Because no strongly emerge. supported phylogenetic placement of Rafflesia has been pro- posed, the understanding of the ancestral conditions facilitating the evolution of its massive flowers and endoparasitic habit has arasitic organisms have evolved independently from free- been hampered. living ancestors in most of the major lineages of prokaryotes P To determine the position of Rafflesia within the context of and eukaryotes (1), but identification of the relatives of highly angiosperm phylogeny we have used mitochondrial (mt) DNA reduced parasites has proven to be a phylogenetic challenge in sequences, which have recently been used to study plant evolu- many cases (2). The evolutionary shift to an advanced parasitic tionary relationships alone or in combination with data from lifestyle is often associated with degeneration of both morphol- other genomic compartments (19–24). One reason for the utility ogies and genomes, leaving few reliable characters with which to of plant mtDNA may be the lower substitution rates that infer phylogenetic relationships (3). In angiosperms, evolution- characterize this genome (25), which seem to provide characters ary relationships of many hemiparasites (parasitic plants that with low levels of homoplasy (20, 24). The low mutation rates of retain the ability to photosynthesize) have recently been clarified mtDNA may facilitate the phylogenetic study of plant parasites (4), largely because they retain vegetative and floral character- as well, because holoparasitic plant 19S mt sequences show only istics linking them to their nonparasitic relatives and because modestly elevated divergences (Ϸ2 times higher) relative to their genomes evolve similarly to nonparasites in rate and photosynthetic plants (26). Here we present the results of a pattern (5). In contrast, inferring the phylogenetic relationships phylogenetic analysis, based on mtDNA sequence variation from of many holoparasitic plants (parasites that can no longer 95 species of seed plants, that strongly places the enigmatic photosynthesize) has been particularly problematic because of holoparasite Rafflesia within angiosperm phylogeny. the reduced vegetative features of holoparasites and genes that may be missing or evolve at extremely high rates under relaxed Methods constraint (3–8). Thus, despite the fact that a comprehensive Using the recent ordinal classification of angiosperms (11) as a framework within which to study angiosperm phylogeny exists, guide, we explicitly sampled at least one family from 43 of 45 provided by combined plastid and nuclear sequences from Ͼ500 species (9–11), the photosynthetic relatives of most holoparasites are currently unknown. This paper was submitted directly (Track II) to the PNAS office. Particularly problematic is the holoparasite Rafflesia (Raffle- Abbreviations: mt, mitochondrial; BS, bootstrap support; JS, jackknife support; PP, poste- siaceae), whose phylogenetic affinities have remained obscure rior probabilities; NJ, neighbor joining; P-BS, parsimony BS; P-JS, parsimony JS. since its description in 1822 (12). Rafflesia, a genus of 20 species, Data deposition: The sequences reported in this article have been deposited in the GenBank is notable for producing the largest flowers in the world, database (accession nos. AY453070–AY453124). measuring up to1mindiameter and weighing up to 7 kg (13). †To whom correspondence should be addressed. E-mail: [email protected]. These massive blooms smell of rotting flesh and attract carrion © 2004 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0305562101 PNAS ͉ January 20, 2004 ͉ vol. 101 ͉ no. 3 ͉ 787–792 Downloaded by guest on September 27, 2021 monophyletic orders to produce a broad mtDNA phylogenetic information on the PNAS web site. Parsimony JS (P-JS) values framework. Sampling included 92 species from 80 angiosperm and NJ-BS values could not be shown in Fig. 1 but are presented families. Of primary interest for this study was the inclusion of below. The complete set of JS values and the NJ tree with BS Rafflesia keithii and its close parasitic relative Rhizanthes zippelii. values are available in Figs. 4 and 5, respectively, which are Both of these species traditionally have been placed in Raffle- published as supporting information on the PNAS web site. In siaceae sensu stricto. Mitrastema yamamotoi (Mitrastemona- general, the P-BS for all nodes obtained with fast stepwise ceae), another extreme holoparasite that has long been placed in addition was lower than the JS, NJ-BS, or PP and may be Rafflesiaceae sensu lato, also was sampled to determine its conservative. The P-BS values and PP shown for each node may phylogenetic affinities. Like Rafflesia, this parasite grows as an therefore be interpreted as the lower and upper bounds of node endophyte within its host (various members of the oak family, reliability, respectively (37). The strict consensus tree suggests Fagaceae), emerging only during flower production (3). Because that the members of the ANITA (Amborella, Nymphaeales, and the morphology of Mitrastema is so divergent from that of Austrobaileyales) clade (19, 22, 23) are the basal-most angio- photosynthetic plants, its affinities have remained obscure, with sperms, followed by an unresolved set of relationships among no relatives ever proposed aside from other endophytic parasites magnoliid orders, including all monocots. Expected major eud- like Rafflesia (27). Three gymnosperms, Pinus, Ginkgo, and icot relationships include monophyletic rosids and asterids. All Zamia, were included as outgroups to root phylogenetic esti- recently recognized orders are monophyletic when represented mates. Table 1, which is published as supporting information on by more than one family, and, in most cases, BS and PP are high the PNAS web site, lists all of the species included in this study, at the ordinal level (Fig. 1). the GenBank accession numbers for all of the sequences ana- Within the context of this global angiosperm mtDNA phylog- lyzed, and the
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