Crassulacean Acid Metabolism and Epiphytism Linked toAdaptive Radiations in the Orchidaceae1[OA]Katia Silvera*, Lo uis S. Santiago, Jo hn C. Cushman, and Klaus WinterBiochemistry and Mol ecular Biology MS 200, University of Nevada, Reno, Nevad a 89557–0200 (K.S., J .C.C.);Smithsonian Tropica l Research Institute, Balboa, Anco´n, Republic of Panama (K.S., K.W.); and Botany andPlant Sciences, University of California, Riverside, California 92521 (L.S .S.)Species of the large family Orchidaceae display a spectacular array of adaptations and rapid speciations that are linked toseveral innovative features, including specialized pollination syndromes, colonization of epiphytic habitats, and the presenceof Crassulacean acid metabolism (CAM), a water-conserving photosynthetic pathway. To better understand the role of CAMand epiphytism in the evolutionary expansion of tropical orchids, we sampled leaf carbon isotopic composition of 1,103 speciesnative to Panama and Costa Rica, performed character state reconstruction and phylogenetic trait analysis of CAM andepiphytism, and related strong CAM, present in 10% of species surveyed, to climatic variables and the evolution of epiphytismin tropical regions. Altitude was the most important predictor of photosynthetic pathway when all environmental variableswere taken into account, with CAM being most prevalent at low altitudes. By creating integrated orchid trees to reconstructancestral character states, we found that C3photosynthesis is the ancestral state and that CAM has evolved at least 10independent times with several reversals. A large CAM radiation event within the Epidendroideae, the most species-richepiphytic clade of any known plant group, is linked to a Tertiary species radiation that originated 65 million years ago. Ourstudy shows that parallel evolution of CAM is present among subfamilies of orchids, and correlated divergence betweenphotosynthetic pathways and epiphytism can be explained by the prevalence of CAM in low-elevation epiphytes and rapidspeciation of high-elevation epiphytes in the Neotropics, contributing to the astounding diversity in the Orchidaceae.Crassulacean acid metabolism (CAM) is a taxonom-ically widespread photosynthetic pathway that hasevolved in plants of CO2- and water-limited environ-ments, includin g tropical forest canopies with inter-mittent or seasonal water availability, hot semiaridregions, and some aquatic environments. The CAMpathway is characterized by the temporal separationof carbon fixation between nocturnal CO2fixation byphosphoenolpyruvate carboxylase in the cytosol anddaytime decarboxylation of organic acids to releaseCO2that is then refixed by Rubisco in the chloroplast(Ting, 1985). CAM photosynthesis is found in approx-imately 7% of vascular plant species from 34 families(Smith and Winter, 1996; Holtum et al., 2007). About10% of all vascular plant species are estimated to beepiphytes (Benzing, 1989), many of which exhibitCAM (Lu¨ttge, 2004). CAM vascular epiphytes (mostlyorchids and bromeliads) are an important componentof the biomass and species richness of tropical forestcanopies (Benzing, 1987; Lu¨ttge, 2004; Zotz, 2004).Bromeliads, aroids, and orchids are three of the veryfew flowering plant lineages that were able to success-fully colonize epiphytic nich es (Gentry and Dodson,1987). Yet, orchids are particularly species-rich relativeto these other epiphytic groups (Gravendeel et al.,2004), making Orchidaceae a prime subject for under-standing me chanisms of evolutionary radiation anddiversification. About 72% of orchid species are esti-mated to be epiphytic (Benzing, 1989; Gravendeelet al., 2004), with the majority of these being restrictedto tropical regions. Tropical forest canopies are rich inepiphytic CAM plant diversity (Benzing, 1987; Winterand Smith, 1996; Lu¨ttge, 2004). CAM has been found in62% and 26% of epiphytic orchid species in Australianand New Guinean rainf orests, respectively (Winteret al., 1983; Earnshaw et al., 1987), 42% of orchidspecies in a moist lowland forest site in Panama (Zotzand Ziegler, 1997), and up to 100% of the epiphyticflora in a Mexican dry forest (Mooney et al., 1989). Theabundance of CAM species in such habitats is relatedto limited water availability. Within a single site, thepercentage of CAM epiphytes increases with canopyheight, from 7% in the forest understory, to 25% at1This work was supported by the Environmental ProtectionAgency (Greater Research Opportunities Graduate Program Assis-tance Agreement no. MA 91685201 to K.S.), the National ScienceFoundation (grant nos. IOB–0543659 to J.C.C. and DEB–0706813 toL.S.S.), the National Institutes of Health (grant no. P20 RR–016464from the Idea Network of Biomedical Research Excellence Program ofthe National Center for Research Resources supporting the NevadaGenomics, Proteomics, and Bioinformatics Center), the Andrew W.Mellon Foundation through the Smithsonian Tropical Research Insti-tute (to K.W.), and the Nevada Agricultural Experiment Station (aspublication no. NAES 03087114).* Corresponding author; e-mail [email protected] author responsible for distribution of materials integral to thefindings presented in this article in accordance with the policydescribed in the Instructions for Authors (www.plantphysiol.org) is:Katia Silvera ([email protected]).[OA]Open Access articles can be viewed online without a sub-scription.www.plantphysiol.org/cgi/doi/10.1104/pp.108.1325551838 Plant Physiology, April 2009, Vol. 149, pp. 1838–1847, www.plantphysiol.org ! 2009 American Society of Plan t Biologistsintermediate heights, to 50% in exposed canopy sites(Zotz and Ziegler, 1997). CAM species are also foundin contrasting habitats such as very arid and verymoist sites, which provides evidence of the biochem-ical flexibility of this photosynthetic adaptation (Doddet al., 2002). Several researchers have postulated that inaddition to CAM, mechanisms such as production ofdust-like seeds capable of long-distance dispersal,germination associations with mycorrhizae, absorp-tive velamentous photosynthetic root tissue capable ofrapid water uptake, and reproductive features thatpromote special ized pollination syndromes have con-tributed to the diversification of epiphytic orchids(Benzing, 1987; Gravendeel et al., 2004; Peakall, 2007;Mondrago´n-Palomino and Theissen, 2008). WhetherCAM is linked to epiphytic diversification and speciesradiations throughout evolutionary time remainspoorly
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