Abstract
Phosphoenolpyruvate carboxylase (PEPC) catalyses the initial fixation of atmospheric CO2 into oxaloacetate and subsequently malate. Nocturnal accumulation of malic acid within the vacuole of photosynthetic cells is a typical feature of plants that perform crassulacean acid metabolism (CAM). PEPC is a ubiquitous plant enzyme encoded by a small gene family, and each member encodes an isoform with specialized function. CAM-specific PEPC isoforms probably evolved from ancestral non-photosynthetic isoforms by gene duplication events and subsequent acquisition of transcriptional control elements that mediate increased leaf-specific or photosynthetic-tissue-specific mRNA expression. To understand the patterns of functional diversification related to the expression of CAM, ppc gene families and photosynthetic patterns were characterized in 11 closely related orchid species from the subtribe Oncidiinae with a range of photosynthetic pathways from C3 photosynthesis (Oncidium cheirophorum, Oncidium maduroi, Rossioglossum krameri, and Oncidium sotoanum) to weak CAM (Oncidium panamense, Oncidium sphacelatum, Gomesa flexuosa and Rossioglossum insleayi) and strong CAM (Rossioglossum ampliatum, Trichocentrum nanum, and Trichocentrum carthagenense). Phylogenetic analysis revealed the existence of two main ppc lineages in flowering plants, two main ppc lineages within the eudicots, and three ppc lineages within the Orchidaceae. Our results indicate that ppc gene family expansion within the Orchidaceae is likely to be the result of gene duplication events followed by adaptive sequence divergence. CAM-associated PEPC isoforms in the Orchidaceae probably evolved from several independent origins.
Highlights
Crassulacean acid metabolism (CAM) is one of three modes of photosynthesis found in vascular plants for the assimilation of atmospheric CO2
We use tropical orchids as a study group, because CAM is widespread among epiphytes within this large family of vascular plants (Winter and Smith, 1996a; Silvera et al, 2009, 2010a, b), and because species within the Orchidaceae exhibit a gradient of photosynthetic pathways ranging from C3 photosynthesis to weak- and strong-CAM modes (Silvera et al, 2005, 2010a)
The phylogenetic relationship of the 11 Oncidiinae species used in this study (Fig. 1) followed the nomenclature proposed by Neubig et al (2012) and is consistent with the phylogenetic relationships within Oncidiinae sensu Chase inferred from 590 species (Neubig et al, 2012)
Summary
Crassulacean acid metabolism (CAM) is one of three modes of photosynthesis found in vascular plants for the assimilation of atmospheric CO2. To gain insight into the evolutionary history of genes recruited for CAM function, the study of taxa containing many closely related species with contrasting photosynthetic pathways is experimentally helpful In this context, we use tropical orchids as a study group, because CAM is widespread among epiphytes within this large family of vascular plants (Winter and Smith, 1996a; Silvera et al, 2009, 2010a, b), and because species within the Orchidaceae exhibit a gradient of photosynthetic pathways ranging from C3 photosynthesis to weak- and strong-CAM modes (Silvera et al, 2005, 2010a). Weak CAM appears to be common among neotropical orchid species (Silvera et al 2005)
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