Crassulacean Acid Metabolism and Epiphytism Linked to Adaptive Radiations in the Orchidaceae1 OA Katia Silvera Louis S Santiago John C Cushman and Klaus Winter Biochemistry and Molecular Biology MS 200 University of Nevada Reno Nevada 89557 0200 K S J C C Smithsonian Tropical Research Institute Balboa Anco n Republic of Panama K S K W and Botany and Plant 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 to several innovative features including specialized pollination syndromes colonization of epiphytic habitats and the presence of Crassulacean acid metabolism CAM a water conserving photosynthetic pathway To better understand the role of CAM and epiphytism in the evolutionary expansion of tropical orchids we sampled leaf carbon isotopic composition of 1 103 species native to Panama and Costa Rica performed character state reconstruction and phylogenetic trait analysis of CAM and epiphytism and related strong CAM present in 10 of species surveyed to climatic variables and the evolution of epiphytism in tropical regions Altitude was the most important predictor of photosynthetic pathway when all environmental variables were taken into account with CAM being most prevalent at low altitudes By creating integrated orchid trees to reconstruct ancestral character states we found that C3 photosynthesis is the ancestral state and that CAM has evolved at least 10 independent times with several reversals A large CAM radiation event within the Epidendroideae the most species rich epiphytic clade of any known plant group is linked to a Tertiary species radiation that originated 65 million years ago Our study shows that parallel evolution of CAM is present among subfamilies of orchids and correlated divergence between photosynthetic pathways and epiphytism can be explained by the prevalence of CAM in low elevation epiphytes and rapid speciation of high elevation epiphytes in the Neotropics contributing to the astounding diversity in the Orchidaceae Crassulacean acid metabolism CAM is a taxonomically widespread photosynthetic pathway that has evolved in plants of CO2 and water limited environments including tropical forest canopies with intermittent or seasonal water availability hot semiarid regions and some aquatic environments The CAM pathway is characterized by the temporal separation of carbon fixation between nocturnal CO2 fixation by phosphoenolpyruvate carboxylase in the cytosol and daytime decarboxylation of organic acids to release CO2 that is then refixed by Rubisco in the chloroplast Ting 1985 CAM photosynthesis is found in approx1 This work was supported by the Environmental Protection Agency Greater Research Opportunities Graduate Program Assistance Agreement no MA 91685201 to K S the National Science Foundation grant nos IOB 0543659 to J C C and DEB 0706813 to L S S the National Institutes of Health grant no P20 RR 016464 from the Idea Network of Biomedical Research Excellence Program of the National Center for Research Resources supporting the Nevada Genomics Proteomics and Bioinformatics Center the Andrew W Mellon Foundation through the Smithsonian Tropical Research Institute to K W and the Nevada Agricultural Experiment Station as publication no NAES 03087114 Corresponding author e mail silverak unr nevada edu The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors www plantphysiol org is Katia Silvera silverak unr nevada edu OA Open Access articles can be viewed online without a subscription www plantphysiol org cgi doi 10 1104 pp 108 132555 1838 imately 7 of vascular plant species from 34 families Smith and Winter 1996 Holtum et al 2007 About 10 of all vascular plant species are estimated to be epiphytes Benzing 1989 many of which exhibit CAM Lu ttge 2004 CAM vascular epiphytes mostly orchids and bromeliads are an important component of the biomass and species richness of tropical forest canopies Benzing 1987 Lu ttge 2004 Zotz 2004 Bromeliads aroids and orchids are three of the very few flowering plant lineages that were able to successfully colonize epiphytic niches Gentry and Dodson 1987 Yet orchids are particularly species rich relative to these other epiphytic groups Gravendeel et al 2004 making Orchidaceae a prime subject for understanding mechanisms of evolutionary radiation and diversification About 72 of orchid species are estimated to be epiphytic Benzing 1989 Gravendeel et al 2004 with the majority of these being restricted to tropical regions Tropical forest canopies are rich in epiphytic CAM plant diversity Benzing 1987 Winter and Smith 1996 Lu ttge 2004 CAM has been found in 62 and 26 of epiphytic orchid species in Australian and New Guinean rainforests respectively Winter et al 1983 Earnshaw et al 1987 42 of orchid species in a moist lowland forest site in Panama Zotz and Ziegler 1997 and up to 100 of the epiphytic flora in a Mexican dry forest Mooney et al 1989 The abundance of CAM species in such habitats is related to limited water availability Within a single site the percentage of CAM epiphytes increases with canopy height from 7 in the forest understory to 25 at Plant Physiology April 2009 Vol 149 pp 1838 1847 www plantphysiol org 2009 American Society of Plant Biologists CAM and Epiphytism in Orchids intermediate heights to 50 in exposed canopy sites Zotz and Ziegler 1997 CAM species are also found in contrasting habitats such as very arid and very moist sites which provides evidence of the biochemical flexibility of this photosynthetic adaptation Dodd et al 2002 Several researchers have postulated that in addition to CAM mechanisms such as production of dust like seeds capable of long distance dispersal germination associations with mycorrhizae absorptive velamentous photosynthetic root tissue capable of rapid water uptake and reproductive features that promote specialized pollination syndromes have contributed to the diversification of epiphytic orchids Benzing 1987 Gravendeel et al 2004 Peakall 2007 Mondrago n Palomino and Theissen 2008 Whether CAM is linked to epiphytic diversification and species radiations throughout evolutionary time remains poorly understood Orchid systematics is now at an advanced stage allowing ancestral state reconstruction and correlated evolution analysis of key
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