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Evolutionary Physiology: the Extent of C4 and CAM Photosynthesis in the Genera Anacampseros and Grahamia of the Portulacaceae Lonnie J

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Evolutionary Physiology: the Extent of C4 and CAM Photosynthesis in the Genera Anacampseros and Grahamia of the Portulacaceae Lonnie J Roger Williams University DOCS@RWU Feinstein College of Arts & Sciences Faculty Feinstein College of Arts and Sciences Publications 2008 Evolutionary Physiology: The extent of C4 and CAM photosynthesis in the Genera Anacampseros and Grahamia of the Portulacaceae Lonnie J. Guralnick Roger Williams University, [email protected] Amanda Cline Monica Smith Rowan F. Sage Follow this and additional works at: http://docs.rwu.edu/fcas_fp Part of the Biology Commons Recommended Citation Guralnick, LJ, Amanda Cline, Monica Smith and Rowan Sage. 2008. "Evolutionary Physiology: The extent of C4 and CAM photosynthesis in the Genera Anacampseros and Grahamia of the Portulacaceae." Journal of Experimental Botany. 59 (7): 1735-1742. This Article is brought to you for free and open access by the Feinstein College of Arts and Sciences at DOCS@RWU. It has been accepted for inclusion in Feinstein College of Arts & Sciences Faculty Publications by an authorized administrator of DOCS@RWU. For more information, please contact [email protected]. Journal of Experimental Botany, Vol. 59, No. 7, pp. 1735–1742, 2008 doi:10.1093/jxb/ern081 Advance Access publication 24 April, 2008 SPECIAL ISSUE RESEARCH PAPER Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae Lonnie J. Guralnick1,*, Amanda Cline1, Monica Smith2 and Rowan F. Sage3 1 Division of Natural Science & Mathematics, Western Oregon University, Monmouth, OR 97361, USA 2 School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA 3 Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S 1A1 Canada Received 11 September 2007; Revised 25 February 2008; Accepted 28 February 2008 Abstract a marked increased phosphoenolpyruvate carboxylase activity. This showed that the Grahamia species are The Portulacaceae is one of the few terrestrial plant actually facultative CAM plants despite their C -like families known to have both C and Crassulacean acid 3 4 carbon isotope values. The results indicate that the metabolism (CAM) species. There may be multiple Grahamia and Anacampseros species do not utilize origins of the evolution of CAM within the Portulaca- the C photosynthetic pathway. This is the first to ceae but the only clear evidence of C photosynthesis 4 4 identify that the Grahamia species are facultative CAM is found in members of the genus Portulaca. In the plants where CAM can be induced by water stress. Portulaca, CAM succulent tissue is overlaid with the C 4 This work supports earlier physiological work that tissue in a unique fashion where both pathways are indicates that this clade containing Anacampseros operating simultaneously. Earlier reports have shown and Grahamia species comprises predominantly facul- that the clade containing the genera Anacampseros tative CAM plants. This report suggests there may be and Grahamia may also contain C4 photosynthetic only one clade which contains C4 photosynthetic species similar to the Portulaca, which would indicate members with CAM-like characteristics. multiple origins of C4 photosynthesis within the family. The aim of the present study was to ascertain the true Key words: Anacampseros, carbon isotope composition, C4 photosynthetic nature of these genera. An initial photosynthesis, Crassulacean acid metabolism (CAM), survey of the carbon isotope composition of the evolution, Grahamia, PEP carboxylase, Portulacaceae. Anacampseros ranged from –12.6& to –24.0&, in- dicating very little CAM activity in some species, with other values close to the C range. Anacampseros 4 Introduction (¼Grahamia) australiana which had been previously identified as a C4 species had a carbon isotope In terrestrial plants, two metabolic adaptations that composition value of –24.0&, which is more indicative concentrate CO2 are known: the C4 and the Crassulacean of a C3 species with a slight contribution of CAM acid metabolism (CAM) pathway of photosynthesis. The activity. Other Anacampseros species with C4-like C4 pathway is found in 19 plant families and ;7000 values have been shown to be CAM plants. The initial species (Sage et al., 1999; Sage, 2001), while CAM has isotope analysis of the Grahamia species gave values evolved in >30 families and occurs in at least 20 000 in the range of –27.1& to –23.6&, placing the Graha- species (Winter and Smith, 1996; Sage and Monson, mia species well towards the C3 photosynthetic range. 1999). Both metabolic pathways evolved independently Further physiological studies indicated increased in well over two dozen distinct lineages (Winter and night-time CO2 uptake with imposition of water stress, Smith, 1996; Sage, 2004), and both pathways have associated with a large diurnal acid fluctuation and evolved in four higher plant families (Aizoaceae, * To whom correspondence should be addressed. E-mail: [email protected] ª The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: [email protected] Downloaded from https://academic.oup.com/jxb/article-abstract/59/7/1735/646297/Evolutionary-physiology-the-extent-of-C4-and-CAM by Roger Williams University user on 11 October 2017 1736 Guralnick et al. Asteraceae, Euphorbiaceae, and Portulacaceae). In one performance by restricting CO2 loss during phase III of family, the Portulacaceae, CAM and C4 evolved in close CAM (Guralnick et al., 1986, 2001; Maxwell et al., 1997; relatives, and can even co-occur in the same species in the Nelson and Sage, 2005). The structural adaptations genus Portulaca. Evolution of CAM and C4 appears to required to effect CAM, and the changes in enzyme occur by different intermediate steps, which may be regulation required to create a CAM diurnal cycle, are two incompatible (Sage, 2002), so the presence of CAM and features which are hypothesized to produce major barriers C4 in a common evolutionary lineage represents an to the origin of CAM and C4 photosynthesis in a common interesting question of significance to the understanding evolutionary lineage. Consistent with this idea, only one of complex trait evolution. of the dozens of evolutionary lineages with CAM or C4 The C4 pathway first evolved 24–35 million years ago has both pathways present. This is the section of the in grasses and later in dicots in response to decreasing Portulacaceae that includes Portulaca, Grahamia, and CO2 concentration in the atmosphere (Sage, 2004; Anacampseros (Hershkovitz and Zimmer, 1997). Christin et al., 2008). The steps involved in the evolution To distinguish C3,C4, and CAM plants within a given of the C4 pathway include the formation of distinct phylogeny, carbon isotope composition values can be mesophyll and bundle sheath (Kranz anatomy) compart- used as an initial indicator to estimate the proportional ments, followed by localization of the photorespiratory contribution of RuBP carboxylase and PEPCase to the enzyme glycine decarboxylase to the bundle sheath overall carbon gain of the plant (Winter and Holtum, (Hylton et al., 1988; Moore et al., 1988; Rawsthorne, 2002). C3 plants will show values of around –29& when 1988; Erhleringer and Monson, 1993; Sage, 2004). This 100% of the CO2 is captured by RuBP carboxylase, with forms a modest CO2 concentration system where oxygen- a less negative upper limit of –23& to –20& due to ation products are shuttled to the bundle sheath for chemical, diffusional, and environmental constraints decarboxylation during photorespiration, with the result (Winter and Holtum, 2002). C4 plants which utilize that CO2 levels are elevated around bundle sheath PEPCase as the initial enzyme to capture CO2 can chloroplasts. Subsequent to this, a C4 cycle is engaged by typically have a range from –10& to –16& (Sage et al., up-regulating phosphoenolpyruvate carboxylase (PEPCase) 2007). CAM plants can range from both ends of the and the expression of the other enzymes in the C4 spectrum depending on the contribution of the CAM pathway. The main evolutionary driver for C4 evolution pathway to the overall carbon gain of the plant. Failure to thus appears to be the scavenging of photorespiratory account for this could lead to a misidentification of CO2, and thus C4 photosynthesis evolves in habitats that a CAM plant as being a C3 or C4, and hence it is usually consistently experience conditions conducive to high necessary to complement carbon isotope analyses with ribulose bisphosphate (RuBP) oxygenase activity by additional physiological investigation to ensure proper Rubisco. Recent work has shown that the Kranz anatomy identification of CAM in a candidate species (Winter and is not essential for terrestrial C4 photosynthesis to occur, Holtum, 2002). but can occur in a single cell with a spatial separation of The Portulacaceae is a medium-sized family with ;30 the C4 and C3 pathway within a single chlorenchyma cell genera and 450 species with a wide distribution, but is (Voznesenskaya et al., 2001, 2002; Edwards et al., 2004). predominant in the Southern hemisphere (Eggli and Ford- CAM photosynthesis occurs in primitive vascular Werntz, 2002). The Portulacaceae has species which are plants, indicating a very ancient origin; however, most of strict C3 plants (typically those found in Western North the modern lineages appear to have arisen in the same America; Guralnick et al., 2001); others which are C3 time frame as the C4 lineages (during the last 35 million plants with some attributes of CAM; others which are C4
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