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Ecology |
Department of Ecology and Evolutionary Biology, Unit 3043, 75 N. Eagleville Road, University of Connecticut, Storrs, Connecticut 06269 USA
Received for publication January 22, 2002. Accepted for publication August 1, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: CAM idling • crassulacean acid metabolism • Geraniaceae • growth form • Pelargonium • phylogeny • southern African plants • succulence
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Mooney, Troughton, and Berry, 1977
; Rundel, Esler, and Cowling, 1999
; Veste, Herppich, and von Willert, 2001
).
The presence of high numbers of succulent plant species in the South African Cape Floristic region (Goldblatt, 1978
) has inspired interest in the occurrence of CAM in the southern African flora. Numbers of plant species in the succulent karoo and fynbos regions exceed Amazonia in some areas (Cowling and Richardson, 1995
) and are accompanied by high endemism, estimated at nearly 70% for the Cape Flora (Bond and Goldblatt, 1984
) and 40–50% in Namaqualand (Cowling, Esler, and Rundel, 1999
). This extraordinary species richness in several clades has been hypothesized to result from explosive, recent radiations in response to increasing aridification caused by the altered flow of ocean currents in the Miocene (Bakker, Culham, and Gibby, 1999
; Richardson et al., 2001
). Consistent with this hypothetical radiation is the large number of species in these regions that are stem succulent, leaf succulent, or geophytic—growth forms whose presence is generally attributed to predictable but limited rainfall. The rapid radiation of species, possibly since the late Miocene and Pliocene, combined with the common occurrence of variations on succulent growth forms, suggests that the South African flora may be particularly useful for studying not only the patterns of occurrence of CAM, but also the evolution of CAM photosynthesis within genera whose phylogenetic relationships are well described.
Pelargonium L'Hérit. ranks as the third largest plant genus in the Cape flora (Goldblatt and Manning, 2000
). It is the sister group to the remainder of the Geraniaceae clade (Price and Palmer, 1993
; Albers, 1996
). Based on limited data (e.g., Thomas and Beevers, 1949
; Schütte, Steyn, and van der Westhuisen, 1967
; Kluge and Ting, 1978
), the Geraniaceae are considered a "minor" CAM family, defined as one in which only a small number of species have CAM photosynthesis or one that contains species that show only weak CAM activity (Winter and Smith, 1996
). Sampling for CAM activity in the family has not been systematic or extensive. The apparent radiation of species within the genus Pelargonium offers unusual potential for exploring the evolution of CAM photosynthesis within a known phylogenetic framework. Species of Pelargonium fall into two main groups that can be distinguished on the basis of chromosome size, biogeographical distribution, and mitochondrial and chloroplast DNA sequences (Bakker et al., 1999
, 2000
; Bakker, Culham, and Gibby, 1999
). The majority of the approximately 280 species of Pelargonium are concentrated in the winter rainfall region of southern Africa, and over 80% of the species in the region are members of a single clade (Clade A in Fig. 1). These species are characterized by growth forms ranging from evergreen shrubs to deciduous subshrubs, stem succulents, and geophytes (for illustrations, see van der Walt, 1977
; van der Walt and Vorster, 1981
, 1988
). The evolution of stem succulence in shrubs and subshrubs appears to have occurred at least three times in Pelargonium (C. S. Jones, unpublished data).
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; Kluge and Ting, 1978
), but Rundel, Esler, and Cowling (1999)
found that both P. crithmifolium and another stem succulent species, P. klinghardtense, had leaf carbon isotope discrimination values typical of C3 photosynthesis. Von Willert et al. (1992)
reported that at least one Pelargonium species they examined (listed as Pelargonium sp.) was a C3 plant, whereas one species of geophyte (also listed as Pelargonium sp.) is "likely to exhibit CAM or CAM cycling." Another species, P. fulgidum, a semisucculent subshrub, did not exhibit diel acid fluctuations (Schütte, Steyn, and van der Westhuisen, 1967
). In order to more systematically evaluate CAM-related patterns of nocturnal acid accumulation and the evolution of carbon metabolism within Pelargonium, we examined dusk/dawn changes in titratable acidity sampled broadly across the genus. We emphasized those species from the winter rainfall region, using a total of 41 species grown under well-watered, greenhouse conditions. These observations were supplemented with investigations of photosynthetic rates and stomatal conductance in selected species and with investigations of plasticity of acid fluctuations and photosynthesis in response to withholding water. We found variation among sections in the tendency toward pronounced increases in nocturnal leaf and stem acidity; we did not find species that had evolved full CAM. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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); the two major groups (defined by small and large chromosomes) will receive subgeneric status. The phylogenetic relationships among sections of the small chromosome clade are based on analyses of chloroplast encoded trnL-F sequences (Bakker, Culham, and Gibby, 1999
; Bakker et al., 1999
). Phylogenetic relationships among sections of the large chromosome clade are based on combined nad1 b/c and trnL-F sequences (Bakker et al., 2000
).
Year 1: survey of species
Forty-one species of Pelargonium were selected from those in greenhouse cultivation at the University of Connecticut, Storrs, Connecticut, USA. (See http://ajbsupp.botany.org/v90/ for accession information; voucher specimens for species examined are deposited in the UConn Herbarium.) All individuals examined had been under greenhouse cultivation for at least 2 yr prior to the first year of this study. Individuals from the UConn greenhouse collection of Kalanchoe blossfeldiana and Crassula lactea (known CAM species), as well as Alternanthera ficoides (a known C3–C4 intermediate), were selected as controls. Except where noted below, plants were watered "normally," which was every 3–5 d during the sampling period in year 1. Plants were sampled for titratable acidity between 22 February 1999 and 30 April 1999. Because the expression of CAM is known to vary with developmental age of leaves of some species (Holthe, Sternberg, and Ting, 1987
; Ting et al., 1993
), only fully expanded leaves were sampled. Leaf disks were punched immediately after sunset and again the following dawn using standard #1 (ten disks per leaf), #2 (2–5 disks were punched per leaf depending on leaf tissue available per species), or #6 (one disk per leaf) cork borers. Three samples, each from different leaves of the same individual, were punched at sunset and sunrise for a total of six samples per plant. Some species of Pelargonium (indicated by hatched and light grey bars in Fig. 1) have leaves that are too finely dissected for disks to be punched so they were cut with scissors, kept fully hydrated on moist towels, and their fresh mass determined to the nearest 0.0001 g within 10 min. Each sample was immediately frozen and stored in liquid nitrogen after removal from the plant (or immediately after weighing).
To determine titratable acidity, each sample was ground with 11 mL of pure water from a Millipore Milli-Q plus Ultrapure Water System (Millipore, Bedford, Massachusetts, USA). Ten mL of the resulting solution were then titrated using 0.01 mol/L NaOH to an endpoint of pH 7.00 with constant mixing. The remaining 1 mL of solution was used to rinse the end of the Orion pH meter probe (model 520A, Orion Research, Beverly, Massachusetts, USA) before beginning the titrations. Titratable tissue acidities are presented as micromoles of H+ per square centimeter fresh tissue or micromole of H+ per milligram fresh mass tissue.
For all data, reported values of P < |t| between dusk (daytime accumulation) and dawn (nighttime accumulation) acidity samples were determined using t tests based on three leaves per plant (except for P. laxum, which was based on two leaves per plant) (PROC t test) (SAS, 1999–2000
).
Year 1: test for CAM induction in leaves
Two stem succulent species, P. carnosum and P. laxum, were tested for acid fluctuations correlated with water stress. Six plants of P. carnosum were used: three were watered normally, and three were denied water for 9 d beyond the normal watering period (i.e., about 12 d). For P. laxum, five individuals were used; three were denied water for 12 d and two were watered normally. On day 12, plants in both groups were sampled at sunset and then the following morning.
Year 2: gas exchange measurements and acidity patterns in stems and leaves
Based on morphology and on acidity measurements taken during year 1, P. carnosum, P. cortusifolium, P. reniforme, and P. tetragonum were selected for gas exchange measurements during May of year 2. Stomatal conductance and photosynthetic rates were logged every 10 min over 24-h periods using two LI-COR 6400 photosynthesis systems (LI-COR, Lincoln, Nebraska, USA) equipped with red/blue light sources and powered by deep cycle marine batteries. Greenhouse air (varying between 
360 and 400 ppm CO2 over the course of the day) was drawn from a large ballast volume to buffer short-term CO2 fluctuations. Light inside the chamber was programmed to track greenhouse light levels, which were measured by quantum sensors mounted on each leaf chamber head. The LI-COR systems were programmed to keep leaf temperature constant at 25°C, but heating was insufficient to keep leaf temperature at this level overnight. Leaf temperatures dipped as low as 17°C for some plants some evenings and temperatures rose as high as 28°C for some plants on some hot days. Plants were well watered. Also during year 2, titratable acidity was measured in leaves and stem cores for P. carnosum, P. crithmifolium (not included in the year 1 study), and P. tetragonum under well-watered conditions. Stem cores approximately 2 mm thick were punched using a #6 core through the periderm and underlying tissues of branches that had been quickly transported to the laboratory. These pieces of tissue were weighed, immediately frozen, and processed as described above for dissected leaves.
Year 3: gas exchange and leaf acidity during dry-down from well-watered to water-stressed conditions
Because our results from years 1 and 2 suggested that CAM flexibility may influence diel acid accumulations, in June of year 3, both photosynthesis and H+ levels were measured simultaneously in the same plants (different leaves) as they progressed from recently watered (i.e., watered that day or the day before) to water-stressed conditions. Diel photosynthetic responses were tracked every third day over the course of a week of sunny days in early June, when no additional water was applied. Acid levels were determined at dusk and dawn at the beginning of this experiment and again at the end. (Limited leaf material in P. tetragonum constrained us to measuring acids only under water-stressed conditions.)
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Nighttime acid accumulation was found scattered across the phylogenetic tree, and data suggest some section-specific patterns. For example, consider sections where four or more species were sampled. Species within Ligularia sensu stricto (s.s.) (in Clade A1a, Fig. 1) are deciduous, slightly succulent subshrubs, and those we studied had finely divided leaves. All species we examined within Ligularia showed a nighttime increase in mean acid levels, though because of variability in the data, fluctuations were statistically significant only for P. oreophilum. Similarly, all species we examined within section Reniformia (in Clade B, Fig. 1), which are evergreen, herbaceous subshrubs, exhibited nighttime acid accumulation. In contrast, no species within section Ciconium (in the large chromosome clade) showed any nighttime acid accumulation; these species are evergreen and herbaceous. Nor were significant nighttime accumulations observed in the clade of evergreen, woody shrubs (sections Pelargonium and Glaucophyllum). All other sections where four or more species were sampled showed mixed patterns of acid accumulation.
Comparisons among sections in overall leaf acidity also showed some section-specific patterns. Most obviously, in section Otidia, containing those species most prominently stem succulent among our collection, leaf acidity per unit area was high during night and day relative to acid levels in leaves of other groups. The only other species with similar leaf acidity levels was P. tetragonum, an herbaceous stem succulent in the large chromosome clade.
Gas exchange, years 2 and 3
Pelargonium carnosum (section Otidia), P. cortusifolium (section Cortusina), P. reniforme (section Reniformia), and P. tetragonum (section Chorisma) were used for gas exchange experiments during years 2 and 3. These species were chosen for several reasons: their leaf shape was amenable to gas exchange measurements, they are members of widely divergent groups within Pelargonium, and each exhibited nocturnal acid accumulation. Results from all species both years were similar, so only results from P. carnosum for year 3 are presented.
Figure 2 shows photosynthetic rates, stomatal conductance, and light levels immediately after watering (Fig. 2A, B), 3 d later (Fig. 2D, E), and 7 d later for P. carnosum (Fig. 2F, G). During dry-down, there was never evidence of nighttime CO2 fixation in any of the four species examined (e.g., Fig. 2A, D, F). A decline in midday stomatal conductance was observed during intermediate stages of water stress (e.g., Fig. 2D); P. reniforme showed nearly complete midday stomatal closure under these conditions (data not shown). Pelargonium carnosum and P. cortusifolium exhibited slight nocturnal stomatal conductance (1 µmol H2O · m–2 · s–1) under well-watered and intermediate conditions (e.g., Fig. 2A, D), but not under water stress (e.g., Fig. 2F). By the sixth day without water, plants had shut down completely.
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Nocturnal acid accumulation in stems vs. leaves
In year 2, under well-watered conditions, acid fluctuations in both leaves and stems were measured for three species (Fig. 3). Nocturnal acid accumulations were proportionately greater in stems than in leaves in each species, although daytime and nighttime values were not significantly different (note that stem values were quantified per unit tissue mass).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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as "low-level CAM cycling" in Periskioideae, a subfamily of Cactaceae. Crassulacean acid metabolism cycling species exhibit typical C3 daytime CO2 fixation via Rubisco and stomatal conductance (e.g., Fig. 2), but also diel cycling of organic acids characteristic of CAM, associated with fixation of nocturnally respired CO2 into organic acids (Ting, 1985
; Patel and Ting, 1987
; Martin, 1996
). There is no nighttime stomatal conductance in CAM cycling. The low-to-moderate levels of nocturnal acid accumulation many Pelargonium species exhibited in year 1, when plants were receiving water in cycles supporting normal plant growth, may reflect intermediate levels of water stress that arise during this watering cycle (Fig. 1).
All four species of Pelargonium selected for gas exchange analyses exhibited C3 photosynthetic traits under well-watered conditions, though P. carnosum and P. cortusifolium maintained low stomatal conductance during nighttime hours. All four species shut down stomatal conductance and C3 photosynthesis during water stress; none exhibited a transition to CAM (e.g., Fig. 2). Nighttime acid accumulation became more pronounced under water stress in P. reniforme, P. carnosum, and P. tetragonum, suggesting a physiology such as CAM idling may be occurring during water stress. Crassulacean acid metabolism idling has been described in CAM species when water stress induces continuous closure of stomata and nocturnal cycling of low levels of organic acids through the CAM pathway (e.g., Holthe, Sternberg, and Ting, 1987
; Ting et al., 1993
; Kraybill and Martin, 1996
). Considered to be a modification of CAM, CAM idling may be a mechanism for maintaining the plant in a physiologically "poised" state during the period of stress, preventing photodamage as well as recapturing respiratory CO2 (Ting, 1985
). More recent experimental analyses have supported this hypothesis (Griffiths et al., 1989
; Martin, 1996
). In Pelargonium, it appears that CAM idling-like behavior is found under water stress in species that otherwise perform C3 photosynthesis under well-watered conditions.
Trends in CAM evolution in angiosperms
Numerous reports from recent studies of both major and minor CAM families (Winter and Smith, 1996
) suggest that some form of CAM flexibility is common. Several investigators have proposed that the primary force driving evolution of the CAM pathway is its function as a CO2 concentrating mechanism, perhaps in response to limited CO2 availability resulting from midday stomatal closure, rather than solely as a mechanism for increasing water use efficiency (e.g., Winter and Smith, 1996
). This is consistent with Ting's hypothesis (1985)
that in the evolution of CAM, diel acid cycling, and the associated activity of PEPc would have preceded nighttime stomatal opening (see also Ehleringer and Monson, 1993
). Full CAM activity then could have evolved further through the shift in the diel pattern of stomatal opening from one that is exclusively daytime (CAM cycling) to one that is predominantly nighttime (obligate CAM), with the potential intermediate step of nocturnal acid fluctuations occurring in conjunction with stomates that open during the day and again at night (also referred to as "CAM intermediacy"). Thus, nocturnal fixation of respired CO2 by PEPc that originated as a physiologically plastic response to drought may have become evolutionarily fixed to differing degrees, and only later may have become associated with nocturnal conductance to varying degrees in different groups of plants.
Evidence for such a scenario is accruing from investigations of CAM activity within explicitly phylogenetic frameworks. In the genus Kalanchoë; (Crassulaceae), the degree of CAM activity parallels evolutionary changes in growth form and habitat (Kluge and Brulfert, 1996
). The phylogenetically more ancestral taxa exhibit CO2 acquisition via a predominantly C3 pathway, whereas the most derived taxa exhibit obligate CAM; intermediate taxa exhibit flexible CAM, with CO2 uptake occurring during the night and day (Gehrig, Rösicke, and Kluge, 1997
). In contrast to earlier assumptions, this phylogenetic analysis suggests a monophyletic origin of CAM activity, i.e., a singly acquired tendency toward carbon fixation via PEPc, present in the more basal taxa, becomes progressively strengthened and associated with nocturnal stomatal conductance in the more derived taxa in Kalanchoë;. Pilon-Smits, 'T Hart, and van Brederode (1996)
have drawn similar conclusions for Sedum and Aeonium, also in the Crassulaceae.
The pattern of CAM activity in other genera and families appears to be similar. The Cactaceae are described as a major CAM family, with many species of obligate CAM plants. Nevertheless, a recent study of two subfamilies of Cactaceae, Pereskioideae and Opuntioideae, showed C3 patterns of carbon uptake and stomatal conductance, with limited nocturnal acid increases in some species. Thus strict C3 photosynthesis or low levels of CAM cycling occurs in Pereskiodeae, a basal clade, under well-watered conditions. Under the same conditions, nocturnal carbon uptake, in association with proportional increases in nocturnal acid levels, occurs in the subfamily Opuntioideae, whose members exhibited obligate CAM, C3-CAM intermediacy, and CAM cycling (Martin and Wallace, 2000
). Members of the third and most highly derived subfamily Cactoideae are generally considered obligate CAM plants (Nobel and Hartstock, 1986
).
Interestingly, a phylogenetic analysis of internal transcribed spacer (ITS) sequences suggests that the Portulacaceae is paraphyletic and that the Cactaceae arises as a clade within it (Hershkovitz and Zimmer, 1997
). A recent analysis of CAM activity in the Portulacaceae shows that those species basal to the Cactaceae, previously considered to be C3, actually exhibit CAM cycling at low levels (Guralnick and Jackson, 2001
). More derived species of Portulacaceae show stronger nocturnal acid accumulations, and some of the most derived species exhibit facultative CAM, where full CAM is induced by water stress. We speculate that additional analyses of basal taxa in the Portulaceae, extending to the Aizoaceae, may reveal a singly acquired tendency toward low levels of CAM cycling as the basal condition in the clade of the Carophyllales containing the Portulaceae, Aizoaceae, and Cactaceae. Multiple origins of nocturnal stomatal conductance and carbon fixation would then have led to the independent origin of full CAM in each of these groups.
CAM evolution in Pelargonium
In an investigation of the functional significance of CAM cycling, Martin (1996, p. 201)
concluded that "plants with CAM cycling may be viewed as C3 plants when well-hydrated and CAM idling plants when stressed." Our observations indicate that this view accurately describes species of Pelargonium, with the caveat that the extent of nocturnal acid accumulation during CAM cycling that occurs prior to CAM idling is at a relatively low level compared to other genera, with the exception of P. tetragonum. However, our observations also suggest that some sections exhibit tendencies toward more pronounced increases in nocturnal acids than others. Species in sections Ciconium in the large chromosome clade, as well as sections Pelargonium and Campylia of Clade A, show very little if any increase in nocturnal acid levels under normal watering regimes. Species of the winter rainfall area in Clade A1 show considerable variation in their tendency to accumulate acids at night; more pronounced accumulations are not necessarily restricted to the stem or leaf succulent species. The more dramatic increases in nocturnal acids in individual species within sections Chorisma, Reniformia, Otidia, and Clade A1a suggest that an enhanced ability to recycle respired CO2 via PEPc may have evolved, or is evolving, independently within each of the major clades within the genus. Whether such accumulations foreshadow the evolution of full CAM will depend on whether nocturnal conductance evolves in these species. Although not yet associated with measureable amounts of external carbon uptake or acid accumulation, very low levels of nocturnal conductance under well-watered conditions, seen in P. cortusifolium and P. carnosum, suggests that an evolutionary shift in carbon metabolism to full CAM within some species of Pelargonium may indeed be possible.
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FOOTNOTES |
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2 Author for reprint requests (cjones{at}uconnvm.uconn.edu
)
3 Current address: Dept. of Earth and Space Sciences, University of California, Los Angeles, 5676 Geology Bldg., Los Angeles, California 90095-1567 USA
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bakker F. T. A. Culham L. Daugherty M. Gibby 1999 A trnL-F based phylogeny for species of Pelargonium (Geraniaceae) with small chromosomes. Plant Systematics and Evolution 216: 309-324[CrossRef][ISI]
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