JXB Advance Access originally published online on April 24, 2008
Journal of Experimental Botany 2008 59(7):1735-1742; doi:10.1093/jxb/ern081
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RESEARCH PAPER |
Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae
1Division of Natural Science & Mathematics, Western Oregon University, Monmouth, OR 97361, USA
2School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA
3Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S 1A1 Canada
* To whom correspondence should be addressed. E-mail: guralnl{at}wou.edu
Received 11 September 2007; Revised 25 February 2008 Accepted 28 February 2008
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Abstract |
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The Portulacaceae is one of the few terrestrial plant families known to have both C4 and Crassulacean acid metabolism (CAM) species. There may be multiple origins of the evolution of CAM within the Portulacaceae but the only clear evidence of C4 photosynthesis is found in members of the genus Portulaca. In the Portulaca, CAM succulent tissue is overlaid with the C4 tissue in a unique fashion where both pathways are operating simultaneously. Earlier reports have shown that the clade containing the genera Anacampseros and Grahamia may also contain C4 photosynthetic species similar to the Portulaca, which would indicate multiple origins of C4 photosynthesis within the family. The aim of the present study was to ascertain the true photosynthetic nature of these genera. An initial survey of the carbon isotope composition of the Anacampseros ranged from –12.6
to –24.0, indicating very little CAM activity in some species, with other values close to the C4 range. Anacampseros (=Grahamia) australiana which had been previously identified as a C4 species had a carbon isotope composition value of –24.0, which is more indicative of a C3 species with a slight contribution of CAM activity. Other Anacampseros species with C4-like values have been shown to be CAM plants. The initial isotope analysis of the Grahamia species gave values in the range of –27.1 to –23.6, placing the Grahamia species well towards the C3 photosynthetic range. Further physiological studies indicated increased night-time CO2 uptake with imposition of water stress, associated with a large diurnal acid fluctuation and a marked increased phosphoenolpyruvate carboxylase activity. This showed that the Grahamia species are actually facultative CAM plants despite their C3-like carbon isotope values. The results indicate that the Grahamia and Anacampseros species do not utilize the C4 photosynthetic pathway. This is the first to identify that the Grahamia species are facultative CAM plants where CAM can be induced by water stress. This work supports earlier physiological work that indicates that this clade containing Anacampseros and Grahamia species comprises predominantly facultative CAM plants. This report suggests there may be only one clade which contains C4 photosynthetic members with CAM-like characteristics. Key words: Anacampseros, carbon isotope composition, C4 photosynthesis, Crassulacean acid metabolism (CAM), evolution, Grahamia, PEP carboxylase, Portulacaceae
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In terrestrial plants, two metabolic adaptations that concentrate CO2 are known: the C4 and the Crassulacean acid metabolism (CAM) pathway of photosynthesis. The C4 pathway is found in 19 plant families and
7000 species (Sage et al., 1999; Sage, 2001), while CAM has evolved in >30 families and occurs in at least 20 000 species (Winter and Smith, 1996; Sage and Monson, 1999). Both metabolic pathways evolved independently in well over two dozen distinct lineages (Winter and Smith, 1996; Sage, 2004), and both pathways have evolved in four higher plant families (Aizoaceae, Asteraceae, Euphorbiaceae, and Portulacaceae). In one family, the Portulacaceae, CAM and C4 evolved in close relatives, and can even co-occur in the same species in the genus Portulaca. Evolution of CAM and C4 appears to occur by different intermediate steps, which may be incompatible (Sage, 2002), so the presence of CAM and C4 in a common evolutionary lineage represents an interesting question of significance to the understanding of complex trait evolution. The C4 pathway first evolved 24–35 million years ago in grasses and later in dicots in response to decreasing CO2 concentration in the atmosphere (Sage, 2004; Christin et al., 2008). The steps involved in the evolution of the C4 pathway include the formation of distinct mesophyll and bundle sheath (Kranz anatomy) compartments, followed by localization of the photorespiratory enzyme glycine decarboxylase to the bundle sheath (Hylton et al., 1988; Moore et al., 1988; Rawsthorne, 1988; Erhleringer and Monson, 1993; Sage, 2004). This forms a modest CO2 concentration system where oxygenation products are shuttled to the bundle sheath for decarboxylation during photorespiration, with the result that CO2 levels are elevated around bundle sheath chloroplasts. Subsequent to this, a C4 cycle is engaged by up-regulating phosphoenolpyruvate carboxylase (PEPCase) and the expression of the other enzymes in the C4 pathway. The main evolutionary driver for C4 evolution thus appears to be the scavenging of photorespiratory CO2, and thus C4 photosynthesis evolves in habitats that consistently experience conditions conducive to high ribulose bisphosphate (RuBP) oxygenase activity by Rubisco. Recent work has shown that the Kranz anatomy is not essential for terrestrial C4 photosynthesis to occur, but can occur in a single cell with a spatial separation of the C4 and C3 pathway within a single chlorenchyma cell (Voznesenskaya et al., 2001, 2002; Edwards et al., 2004).
CAM photosynthesis occurs in primitive vascular plants, indicating a very ancient origin; however, most of the modern lineages appear to have arisen in the same time frame as the C4 lineages (during the last 35 million years). CAM is more taxonomically diverse than C4 photosynthesis, with many CAM lineages scattered across many monocot and dicot families (Winter and Smith, 1996; Sage, 2004). CAM photosynthesis appears to have originated as a means to scavenge respiratory CO2 under conditions where the carbon balance is restricted in environments where water availability becomes restricted temporarily or seasonally, such as in deserts or rock outcrops, or as in epiphytes. As with C4, CAM involves major changes to the leaf structure as well as metabolism. Succulence is the obvious structural innovation as it facilitates the capture of night-time CO2 released by respiration (Gibson, 1982; Ting, 1985; Sage, 2002); however, tight packing of the mesophyll cells is another key structural feature that appears to enhance CAM performance by restricting CO2 loss during phase III of CAM (Guralnick et al., 1986, 2001; Maxwell et al., 1997; Nelson and Sage, 2005). The structural adaptations required to effect CAM, and the changes in enzyme regulation required to create a CAM diurnal cycle, are two features which are hypothesized to produce major barriers to the origin of CAM and C4 photosynthesis in a common evolutionary lineage. Consistent with this idea, only one of the dozens of evolutionary lineages with CAM or C4 has both pathways present. This is the section of the Portulacaceae that includes Portulaca, Grahamia, and Anacampseros (Hershkovitz and Zimmer, 1997).
To distinguish C3, C4, and CAM plants within a given phylogeny, carbon isotope composition values can be used as an initial indicator to estimate the proportional contribution of RuBP carboxylase and PEPCase to the overall carbon gain of the plant (Winter and Holtum, 2002). C3 plants will show values of around –29 when 100% of the CO2 is captured by RuBP carboxylase, with a less negative upper limit of –23 to –20 due to chemical, diffusional, and environmental constraints (Winter and Holtum, 2002). C4 plants which utilize PEPCase as the initial enzyme to capture CO2 can typically have a range from –10 to –16 (Sage et al., 2007). CAM plants can range from both ends of the spectrum depending on the contribution of the CAM pathway to the overall carbon gain of the plant. Failure to account for this could lead to a misidentification of a CAM plant as being a C3 or C4, and hence it is usually necessary to complement carbon isotope analyses with additional physiological investigation to ensure proper identification of CAM in a candidate species (Winter and Holtum, 2002).
The Portulacaceae is a medium-sized family with 30 genera and 450 species with a wide distribution, but is predominant in the Southern hemisphere (Eggli and Ford-Werntz, 2002). The Portulacaceae has species which are strict C3 plants (typically those found in Western North America; Guralnick et al., 2001); others which are C3 plants with some attributes of CAM; others which are C4 plants which also display some CAM characteristics; and other species which are facultative CAM plants (switching between C3 and CAM photosynthesis). Hence, with respect to photosynthesis, the Portulacaceae is one of the most diverse plant families in the plant kingdom. The only genus known to have C4 photosynthetic members is the genus Portulaca, which forms a distinct clade in the Anacampseroid section (Hershkovitz and Zimmer, 1997). Portulaca most probably evolved the C4 pathway from CAM ancestors (Guralnick and Jackson, 2001). Prior research has shown that Portulaca grandiflora has both the C4 and CAM pathway operating simultaneously in the mesophyll leaf tissue (Guralnick et al., 2002); however, the two pathways are segregated into distinct tissue regions. CAM resides in succulent cells positioned towards the interior of the leaf, while C4 is localized to a few layers of mesophyll cells towards the exterior of the leaf and near the stomata (Guralnick and Jackson, 2001).
The Anacampseroid clade which contains both C4 and CAM members is composed of two subclades; one containing the genus Portulaca and the other subclade containing the genera Anacampseros, Grahamia, Talinopsis, Xenia, and Tallinaria which contains many facultative CAM plants (Hershkovitz and Zimmer, 1997; Guralnick and Jackson, 2001). In addition, earlier reports in the literature have indicated that Grahamia bracteata and two Anacampseros species, A. kurtzii and A. australiana (which have since been placed in Grahamia; Nyffeler, 2007), may also be C4 photosynthetic species (Kellogg, 1999). This raises the possibility of multiple origins of C4 photosynthesis overlaying CAM tissue within the Anacampseroid clade. The placement of the genus Grahamia and Anacampseros as having C4 members is not clearly resolved, as much of the early evidence of a C4 pathway may be incorrect due to the possible operation of a CAM pathway (Watson and Dallwitz, 1992). In this study, the objective is to clarify and identify the photosynthetic pathway utilized within Grahamia and Anacampseros using carbon isotope assessment, gas exchange, titratable acidity analysis, and biochemical assays of PEPCase activity. The results will aid in clarifying the origins of C4 and CAM photosynthesis within the Portulacaceae, thereby allowing for better understanding of how two seemingly incompatible traits might arise in a common evolutionary lineage.
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Materials and methods |
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Plant material
Cuttings of G. bracteata, G. coahuilensis, G. frutescens, and A. vulcanensis were obtained from the Museum of Succulents (Zurich, Switzerland). Plants were then transplanted into pots in a glasshouse. Anacampseros australiana (also known in the literature as Grahamia australiana) plants were purchased from the Rare Plant Research Institute (Portland, OR, USA). All plants grown were irrigated with 1/2 strength Hoagland's solution and irrigated prior to sampling. The plants were grown under natural light conditions supplemented with artificial light to maintain a light level of 400–600 mmol m–2 s–1. The day/night temperature in the glasshouse was 27/17 °C. Water was withheld for 5 d prior to sampling for the water stress conditions. The carbon isotope composition was assessed for all of the living material in the study, and a series of specimens of Anacampseros collected from herbarium sheets at the Royal Botanical Garden at Kew, UK (Table 1). The
13C of living specimens was collected from leaves, ground to a fine powder, and sent to Washington State University (College of Sciences Stable Isotope Core; http://www.isotopes.wsu.edu). Herbarium specimens were analysed at the Stable Isotope centre of the University of California, Davis (http://stable-isotopes.geology.ucdavis.edu). In addition, leaf material of plants of known photosynthetic pathways also growing under the same conditions was collected and sent along with the Grahamia species. Carbon isotope fractionation values were determined on leaf samples taken from plants using a standard procedure relative to PDB (Pee Dee Belemnite) limestone as the carbon isotope standard (Bender et al., 1973).
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Titratable acidity
Three to six leaves were collected in the morning and evening, and were frozen (–20 °C) until assayed. Leaf samples were weighed, ground in glass-distilled water, and titrated with 0.01 N KOH to a pH 7 end-point.
PEPCase activity
Approximately 0.5 g of leaf tissue for PEPCase activity was collected in triplicate in the afternoon under well-watered and water-stress conditions. The samples were assayed spectrophotometrically by following the oxidation of NADH at 340 nm as previously described (Guralnick and Ting, 1987).
CO2 uptake
Rates of photosynthesis were measured with an LCpro+ portable infrared CO2 gas analyser from ADC BioScientific Ltd, Great Amwell, UK, using the conifer chamber. The plants were measured over 24 h with a 16 h photoperiod. Light was increased/decreased stepwise at the beginning and end of the photoperiod, respectively, with a maximum light intensity of 500 PPFD (photosynthetic photon flux density). The source of light was an LCpro+ conifer chamber red and blue LED lamp attachment. Other conditions were set on ambient mode with diurnal temperatures approximating 25/21 °C, 370 ppm CO2, and 50% relative humidity. The area of the leaf was determined using ImageJ 1.36b software from the National Institutes of Health, Bethesda, MD, USA.
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Results |
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Carbon isotope composition
The carbon isotope analysis showed G. bracteata with a value of –23.7
, G. coahuilensis –24.1, A. australiana –24.0, and G. frutescens –26.8 (Table 1). The Anacampseros species showed a wide range of isotope values from –12.6 to –24. The carbon isotope composition values were shifted towards the C4 range, with 18 of the 24 species having values of less than –20. For comparison, the CAM cycling species, Lewisa cotyledon, had a value of –25.2 while the C3 Montia sibirica had a value of –32.6. Two known facultative CAM species, A. rufescens and A. vulcanensis, had rather different carbon isotope values of –17.8 and –23.7, respectively. The C4 species, Portulaca oleracea, had a carbon isotope composition of –13.5. Due to a lack of plant material of A. australiana (except where noted) and G. frutescens, the following results are for G. bracteata and G. coahuilensis.
Titratable acidity
Well-watered plants of G. bracteata, A. australiana, and G. coahuilensis showed very high titratable acidity levels of >200 µeq g–1 FW and little or no diurnal acid fluctuations (Table 2). During the imposition of water stress, both G. bracteata and G. coahuilensis showed a large diurnal acid fluctuation. Grahamia bracteata had a fluctuation of >200 µeq g–1 FW, while G. coahuilensis showed a diurnal acid fluctuation of 148 µeq g–1 FW. Anacampseros australiana showed a smaller diurnal acid fluctuation increase of 58 µeq g–1 FW. All three Grahamia species under water-stress conditions showed a significant difference from the am to pm acid levels.
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PEPCase activity
The well-watered plants of G. bracteata and G. coahuilensis had PEPCase activity of 28–36 µmol mg–1 chl h–1 (Table 2) while A. australiana had a slightly higher activity of 125 µmol mg–1 chl h–1. After imposing 5 d of water stress, G. bracteata and G. coahuilensis both showed a significant induction of enzyme activity, with a 16–26-fold increase in the PEPCase activity (P <0.05, Table 2). Anacampseros australiana did not show a large induction of PEPCase activity when compared with the other plants under water-stress conditions.
CO2 gas exchange
Gas exchange activity of control plants of G. bracteata showed daytime CO2 uptake between 10 µmol m–2 s–1 and 15 µmol m–2 s–1 over the course of the light period (Fig. 1A). At night there was a net loss of CO2 due to respiration. Imposing water stress triggered a change in the CO2 uptake pattern, with primarily night-time CO2 uptake and daytime uptake at the beginning and end of the light period (Fig. 1B). During most of the light period there was little if any net CO2 gas exchange observed.
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Gas exchange activity of control plants of G. coahuilensis also showed daytime CO2 uptake between 10 µmol m–2 s–1 and 15 mol m–2 s–1 over the course of the light period (Fig. 2A). After 3 d of water stress, in G. coahuilensis there was no observable shift to night-time CO2 uptake (Fig. 2B). Water stress imposed for 9 d caused a dramatic decrease in daytime CO2 uptake with very little increase in nocturnal CO2 uptake (Fig. 2B). Early morning and late afternoon uptake remained quite positive after 9 d of water stress.
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Discussion |
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A number of interesting questions arise from studies of the Portulacaceae; how did the C4 and CAM pathway evolve within the Portulacaceae, are there multiple origins, and how may have C4 and CAM evolved in the same species, particularly within a common leaf tissue. Many of the C4 species within the Portulacaceae are also succulent, with increased titratable acidity levels compared with typical C4 species (Kraybill and Martin, 1996; Guralnick et al., 2002). Since both pathways require the same suite of enzymes to function, understanding how these pathways evolved in this family and in the same leaf tissue could reveal important insights into how complex metabolic pathways modify common enzyme systems to serve distinct metabolic roles.
Prior work studying the Portulacaceae demonstrates that CAM evolved from their C3 ancestors to weak CAM first, followed by the formation of facultative CAM in more derived lineages (Guralnick and Jackson, 2001). Facultative CAM metabolism may have multiple origins within the family. The C4 pathway appears to have evolved after CAM, possibly by the modification of a distinct layer of Kranz tissue that is separate from the CAM tissue in leaves of Portulaca species (Guralnick and Jackson, 2001). Additional reports in the literature for the Portulacaceae noted that the genus Trianthema has C4 species, but this genus is now properly placed in the Aizoacaceae (Watson and Dallwitz, 1992). Early reports also indicated that certain Anacampseros species have the C4 pathway, but there is little supporting evidence for this conclusion (Watson and Dallwitz, 1992). A recent phylogenetic analysis demonstrates that Anacampseros is closely aligned to Grahamia and indicates that certain Grahamia species, including the putative C4 species, should be reclassified as Grahamia (Fig. 3; Nyffeler, 2007). Based on this phylogenetic analysis and the close alignment of the C4 photosynthetic Anacampseros with the other members of the genus Grahamia, a physiological investigation was initiated to explore the possibility of multiple origins of C4 photosynthesis and to determine the true photosynthetic characteristics of the genus Anacampseros and Grahamia in the Portulacaceae.
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The initial analysis of the carbon isotope composition of Anacampseros ranged from –12.6
to –24.0, indicating that very little CAM activity is present in some species, while others have values close to the C4 range, indicating either the presence of a C4 pathway or strong CAM activity. While the presence of C4 photosynthesis in species with C4-like isotope values, such as A. arachnoids and A. papyracea, cannot definitively be ruled out, there was little additional evidence that these species are C4. A superficial examination of Anacampseros herbarium material showed no sign of Kranz anatomy (R Sage, personal observation). Kranz anatomy in C4 plants is often readily observed in leaves by examining them when backlit by a strong light, or by viewing the veins on end in cut sections using a strong hand lens or dissecting scope. Also, the presence of 13C values that are intermediate between C3 and C4 values in many of the Anacampseros species is commonly observed in CAM lineages, but not in C3 and C4. Notably, Anacampseros species which had carbon isotope composition values close to the C4 range have been previously shown to be facultative CAM species. Anacampseros filamentosa showed –13.0 here, but previously showed a value of –15.4 in the field (Mooney et al., 1977), and exhibits a large diurnal acid fluctuation when grown under glasshouse conditions (Guralnick and Jackson, 2001). Anacampseros albissima had a variable carbon isotope value from –14.5 to –19.0 and also has been shown to have a diurnal acid fluctuation typical of many CAM species (Kluge and Ting, 1978). Many other Anacampseros species (A. tomentosa, A. dielsiana, A. marlothi, A. telephiastrum, A. retusa, A. minutum, A. lanceolata, A. crinitia, and A. rufescens) have also shown diurnal acid fluctuations typical of facultative CAM species (Guralnick and Jackson, 2001). Together, these results are consistent with the conclusion that these Anacampseros species are mostly likely CAM species with varying contributions of the CAM pathway to the carbon isotope composition of the species.
Within the other Anacampseros clade (Hershkovitz and Zimmer, 1997) are found A. kurtzii and A. australiana, putative C4 species (Watson and Dallwitx, 1992; Kellogg, 1999), Grahamia bracteata, and Xenia (=Anacampseros=Grahamia) vulcanensis which have not been identified regarding which photosynthetic pathway they utilize. Anacampseros (=Grahamia) australiana has a carbon isotope composition value of –24.0, which is more indicative of a C3 species with a slight contribution of CAM activity. The carbon isotope composition values of both G. bracteata and X vulcanensis were of –23.7, which is not indicative of C4 photosynthesis. The other Grahamia species tested ranged from a value of –26.8 to –24.1. These data indicated that these Grahamia species are not C4 plants, with the carbon isotope composition being too negative and not in the C4 range. The results also indicated a minimal contribution of the CAM pathway during its growth, with the carbon isotope composition values being closer to those of C3 plants (Winter and Holtum, 2002). The ranges of carbon isotope composition values obtained were similar to the CAM cycling species, L. cotyledon (Table 1; Guralnick et al., 2001). The isotope data are consistent with the possibility that the Grahamia species are facultative CAM plants because the values are similar to those of the facultative CAM species Portulacaria afra when grown under well-watered conditions (Guralnick and Ting, 1987); however, to be certain, direct physiological assessments are required. Therefore, a physiological investigation was undertaken to ascertain the true nature of the photosynthetic pathway utilized by the Grahamia species.
The well-watered Grahamia plants had very high titratable acidity levels and low levels of PEPCase activity (Guralnick et al., 1984; Guralnick and Ting, 1987). After 5 d of water stress, a large diurnal acid fluctuation was noted, as was a sizable increase of PEPCase activity in A. australiana, G. bracteata, and G. coahuilensis. The gas exchange pattern observed for water-stressed G. bracteata showed a typical CAM pattern with little or no midday CO2 uptake. These results were similar to pre-drought and post-drought patterns of photosynthesis found in P. afra (Guralnick et al., 1984; Guralnick and Ting, 1987).
Grahamia coahuilensis was different from G. bracteata in its response to water stress. Grahamia coahuilensis did not have an increase in nocturnal CO2 uptake as observed in G. bracteata. After 9 d of water stress, the gas exchange data showed only a slight positive increase of night-time CO2 uptake; overall, however, night-time gas exchange remained close to zero while early morning and late afternoon CO2 uptake remained high. The large diurnal acid fluctuation may be explained by substantial night-time refixation of respiratory CO2 by PEPCase, with a relatively small contribution from fixation of atmospheric CO2. This pattern has been observed in other Portulacaceae species such as P. grandiflora (Guralnick et al., 2002), and is commonly referred to as the CAM idling mode. CAM idling is often proposed as an initial phase in the evolution of the CAM pathway. The results support the conclusion that the Grahamia species are weak to strong facultative CAM plants where CAM can be induced by water stress. Based on the carbon isotope composition values, it can be concluded that the genus Grahamia does not utilize the C4 photosynthetic pathway.
The data in this study support the hypothesis that C4 photosynthesis within the Portulacaceae only originated in Portulaca. The clade containing the genera Anacampseros, Talinopsis, and Tallinaria which branches off from a common ancestor shared with Portulaca provides no evidence for C4 species, and should be considered as being C3, weak CAM, or facultative CAM species. These physiological results are similar to what has been observed in the closely aligned Talinopsis genera which had a carbon isotope value of –25.3 (LJ Guralnick, unpublished data) and a large diurnal acid fluctuation (Guralnick and Jackson, 2001).
There still may be multiple origins of C4 photosynthesis within the Portulacaceae. Two apparent clades are present in Portulaca based on morphological and biochemical features. The P. grandiflora type has succulent, tubular leaves and an NADP-ME (malic enzyme) type of C4 photosynthesis, while the P. oleracea type has succulent, flattened leaves with NAD-ME photosynthesis. NADP-ME and NAD-ME are often thought to represent distinct origins because the different biochemical and structural requirements of each subtype appear to preclude one type giving rise to another; however, this hypothesis does require validation (Muhaidat et al., 2007). Phylogenetic resolution is needed to confirm separate origins of the C4 pathway in Portulaca, and possibly to indicate the immediate ancestors of the C4 lineage(s). At present, there is no evidence for C3–C4 intermediacy in Portulaca or its relatives, nor for CAM–C4 intermediacy, and it is not clear what the immediate ancestral genus is, since numerous genera such as Portulacaria and Cistanthe resolve as sister to Portulaca in recent phylogenies (Fig. 3). Because Portulaca represents the possible independent evolution of distinct biochemical and structural subtypes from a common CAM ancestor, the elucidation of phylogenetic relationships in this clade should be an important contribution to understanding photosynthetic pathway evolution in higher plants.
In conclusion, this report shows that A. australiana is not a C4 species but does demonstrate attributes of CAM photosynthesis. It is also shown that G. bracteata is a facultative CAM species that does not utilize the C4 photosynthetic pathway, and most Anacampseros species exhibit carbon isotope ratios that are consistent with this group also being facultative CAM and not C4. It can therefore be recommended that follow-up work on C4 evolution in the Portulacaceae should focus on Portulaca and its immediate ancestors. By identifying patterns of ancestry, a well-resolved phylogeny could allow researchers to focus their efforts on the branch-point species where important evolutionary developments occurred.
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Acknowledgements |
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The authors would like to thank Dr Urs Eggli and the Museum of Succulents (Zurich, Switzerland) for their donation of plants to this study. We thank Dr Gerald Edwards and Washington State University for analysis of the carbon isotope composition. The research was supported in part from the Provost fund for division chairs to LJG and a Cummins Math-Science Western Foundation scholarship to AC. This work was also supported by an NSF-ROA award (DEB-0719322) to LJG and Dr John Cushman, University of Nevada, Reno. LJG would like to thank two anonymous reviewers for their helpful comments on earlier versions of the manuscript.
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