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Systematics and Phytogeography |
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2 Canada; Section of Evolution and Ecology, University of California, Davis, California 95616 USA; Nees-Institute for Biodiversity of Plants, Universität Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany
Received for publication January 19, 2007. Accepted for publication October 9, 2007.
ABSTRACT
C4 photosynthesis evolved multiple times in the Amaranthaceae s.s., but the C4 evolutionary lineages are unclear because the photosynthetic pathway is unknown for most species of the family. To clarify the distribution of C4 photosynthesis in the Amaranthaceae, we determined carbon isotope ratios of 607 species and mapped these onto a phylogeny determined from matK/trnK sequences. Approximately 28% of the Amaranthaceae species use the C4 pathway. C4 species occur in 10 genera—Aerva, Amaranthus, Blutaparon, Alternanthera, Froelichia, Lithophila, Guilleminea, Gomphrena, Gossypianthus, and Tidestromia. Aerva, Alternanthera, and Gomphrena contain both C3 and C4 species. In Aerva, 25% of the sampled species are C4. In Alternanthera, 19.5% are C4, while 89% of the Gomphrena species are C4. Integration of isotope and matK/trnK data indicated C4 photosynthesis evolved five times in the Amaranthaceae, specifically in Aerva, Alternanthera, Amaranthus, Tidestromia, and a lineage containing Froelichia, Blutaparon, Guilleminea, Gomphrena pro parte, and Lithophila. Aerva and Gomphrena are both polyphyletic with C3 and C4 species belonging to distinct clades. Alternanthera appears to be monophyletic with C4 photosynthesis originating in a terminal sublineage of procumbent herbs. Alpine C4 species were also identified in Alternanthera, Amaranthus, and Gomphrena, including one species (Gomphrena meyeniana) from 4600 m a.s.l.
Key Words: alpine • Alternanthera • Amaranthaceae • C4 photosynthesis • Gomphrena
Currently, 19 families of higher plants are known to contain species expressing the C4 photosynthetic pathway. In each family, the C4 pathway arose independently, producing approximately 50 distinct evolutionary lineages (Sage, 2004
; Muhaidat et al., 2007
). Sixteen of these families are eudicots. The eudicot clade with the largest number of C4 species is the Amaranthaceae/Chenopodiaceae alliance, with half of the approximately 1400 eudicot C4 species. The monophyly of the alliance has been well established, although relationships among its major lineages are not yet clear (Manhart and Rettig, 1994
; Downie et al., 1997
; Cuénoud et al., 2002
; Kadereit et al., 2003
; Müller and Borsch, 2005a
). The major lineages are the family Amaranthaceae (as in the circumscription of Schinz, 1893
), the subfamily Polycnemoideae (currently classified within Chenopodiaceae; Ulbrich et al., 1934
; Kühn et al., 1993
), and the chenopod lineages Betoideae, Chenopodioideae-Corispermoideae, and Salicornioideae-Salsoloideae-Suaedoideae (Kadereit et al., 2003
; Müller and Borsch, 2005a
). It has been proposed that the name Amaranthaceae should be applied to all species in the alliance (Amaranthaceae s.l., Baillon, 1887
; Malligson, 1922
; APG, 2003
). However, because recent molecular studies cannot exclude the monophyly of Amaranthaceae s.s. and Chenopodiaceae, these family names are often maintained (Kadereit et al., 2003
; Welsh et al., 2003
; Müller and Borsch, 2005a
; Kapralov et al., 2006
). The chenopodiaceous lineages comprise the largest number of C4 eudicot species (about 500; Sage et al., 1999
). The Amaranthaceae s.s. contains the next highest number, previously estimated to be around 250 C4 species (Sage et al., 1999
).
Comprehensive surveys of the occurrence of C4 photosynthesis in eudicot families have focused on the Chenopodiaceae, most notably the tribes Salsoleae and Suaedeae (Akhani et al., 1997
; Pyankov et al., 1997
, 2001a
, b
; Schütze et al., 2003
). In these tribes, there is strong evidence for multiple evolutionary origins of the C4 pathway, as indicated by variation in leaf anatomy, biochemical metabolism, and the occurrence of the C4 species on separate branches of molecular-based phylogenetic trees (Pyankov et al., 2001a
, b
; Kadereit et al., 2003
). By contrast, little work on the distribution of C4 photosynthesis in the Amaranthaceae s.s. has been reported since initial surveys were conducted three decades ago (Downton, 1975
; Raghavendra and Das, 1978
; Ziegler et al., 1981
). These initial surveys were incomplete because they mainly examined common species and often reported only those with C4 photosynthesis. Without a clear picture of whether species are C3, C4, or intermediate between C3 and C4, it is impossible to assess where the transition from C3 to C4 photosynthesis occurs. Multiple origins appear likely because of the occurrence of known C4 species in different tribes that also contain C3 species (Sage, 2004
; Kadereit et al., 2003
). In the Amaranthaceae, three independent origins of C4 photosynthesis were inferred from a phylogeny based on rbcL sequences, (Kadereit et al., 2003
). More recently, phylogenetic analyses using additional taxa and matK/trnK sequences were able to better resolve relationships within the Amaranthaceae s.s. and revealed the presence of previously unknown clades (Müller and Borsch, 2005a
, b
). With this matK/trnK data, we can now more precisely map C4 species onto the Amaranthaceae tree. To do this, however, a detailed survey of the presence of C3 and C4 photosynthesis in the genera of the Amaranthaceae is required.
Here, we present results of a comprehensive survey of the Amaranthaceae s.s. for C3 and C4 photosynthesis. Our approach was to sample herbarium specimens for stable carbon isotope ratio (
13C). C4 plants have 13C values between –10
and –15, while C3 species generally have 13C values between –20 and –33 (Ehleringer et al., 1997
). Because C4-like carbon isotope ratios also occur in CAM species, we also examined the leaves for the presence of succulence and Kranz anatomy to rule out the possibility that the isotopic value was due to CAM photosynthesis. In total, we examined over 600 of the 900 or so species in the Amaranthaceae s.s. (Townsend, 1993
). Moreover, using matK/trnK sequence data, we inferred a phylogenetic tree with taxon sampling extended to better match the C4 species in our isotope survey.
MATERIALS AND METHODS
Sampling strategy and material
Samples were collected from herbarium specimens in the collections of the Australian National Herbarium, Canberra, Australia (CANB); the Arnold Arboretum (AH) and Grey Herbarium (GH) at Harvard University, Cambridge, Massachusetts, USA; the herbarium of the Charles Darwin University at Palmerston, NT Australia (DNA-NT); the Missouri Botanical Garden, St. Louis, Missouri, USA (MO); the New York Botanical Garden (NY) New York, USA; and the Royal Botanical Gardens, Kew, Richmond, UK (K). Additional samples were investigated from the Amaranthaceae research collection at the herbaria of the Nees-Institute, University of Bonn (BONN) and the University of Texas, Austin (TEX). A list of the specimens sampled is provided in Appendixes S1–S3 (see Supplemental Data with the online version of this article).
Kranz anatomy and isotope analysis
Sampling consisted of first illuminating the back of the herbarium sheet with a microscope lamp to highlight the leaf venation. Venation was examined with a 20x hand lens, and if the leaf had large, dark veins with small aereoles, it was recorded as having Kranz anatomy. Leaves with small, clear veins with relatively large interveinal areas were recorded as lacking Kranz anatomy. After venation was recorded, a small piece (<10 mg) of leaf, stem, or root tissue was removed from the herbarium sheet, or if available, from a packet of loose material attached to the sheet. Samples were stored in microcentrifuge tubes until placed in a tin sample cup (#D1008, Elemental Microanalysis, Okehampton, UK) and sent to the University of California, Davis mass spectrometer facility for isotopic analysis (http://stableisotopefacility.ucdavis.edu). Samples were analyzed with a mass spectrometer using a Pee Dee Belamnite limestone standard. Two or more different herbarium specimens were examined when available. If sampling was not permitted (as with type specimens or sheets with little material), the venation pattern was examined and reported if it was obviously Kranz or non-Kranz.
Molecular phylogenetics
The distribution of C4 photosynthesis was plotted on a tree obtained from parsimony analyses of a combined matK/trnK data set. Most sequences were taken from Müller and Borsch (2005a, b), but the sequences for Pedersenia and Xerosiphon were from the lab of T. Borsch (unpublished data). The sequences for Aerva sanguinolenta, Alternanthera altacruzensis, Al. flavescens, Al. microphylla, Amaranthus asplundii, and Am. viridis were generated for this study using methods described in Müller and Borsch (2005a)
. See Appendix S4 (with Supplemental Data in online version of this article) for specimen information. Alignment of length variable sequences followed the rules described in Löhne and Borsch (2005)
using PhyDE (Müller et al., 2006). From the overall matrix of 2856 positions, five mutational hotspots had to be excluded (H1 = position [pos.] 543–577, H2 = 639–727, H3 = 899–929, H4 = 1536–1538, H5 = 2603–2628) that corresponded to hotspots found in earlier analyses. The resulting matrix comprised 2672 positions from which 492 were variable plus 716 that were variable and parsimony informative. Three inversions were detected (pos. 166–185 of the 5' trnK intron in Al. caracasana and Al. pungens; pos. 249–257 of the matK CDS in Pfaffia fruticulosa; pos. 600–602 in many taxa, = HS 4). The first two indels were reverse-complemented before analysis following Löhne and Borsch (2005)
, whereas the third was excluded because of its oscillating nature (Borsch and Quandt, in press
). Indels were coded in a separate, binary matrix using the simple indel-coding approach as implemented in the program SeqState (Müller, 2004
). The sequence data set (trnK group II intron and matK gene) and the indel matrix were combined for all analyses because earlier studies had shown that individual trees did not conflict in Amaranthaceae and that indels are phylogenetically informative (Müller and Borsch, 2005a
). Maximum parsimony searches were conducted with the ratchet algorithm (Nixon, 1999
) by creating command files with the program PRAP (Müller, 2004
) and executing them in the program PAUP* (Swofford, 1998
). Ratchet settings were 10 random addition cycles in 200 iterations each, with the weight of 25% perturbed characters = 2. Node support was calculated via jackknifing (10 000 replicates, 36.8% character deletion, heuristic searches holding only one tree). The distribution of C4 photosynthesis was then plotted on tree number one obtained by parsimony using the program Mesquite 1.12 (Maddison and Maddison, 2006
).
Taxonomic treatment
Circumscription of genera largely follows Townsend (1993)
with modifications indicated by recent molecular phylogenies (Müller and Borsch, 2005a
, b
). Our treatment also reflects results of phylogenetic work in progress such as the study of Iresine and relatives (T. Borsch lab, unpublished data). To obtain an up-to-date species nomenclature, we used several recent checklists and floras, including the Catálogo de las Plantas Vasculares de la República Argentina (Pedersen, 1999
), Flora of Ecuador (Eliasson, 1987
), Catálogo de las Plantas Vasculares de Peru (Borsch, 1993
), Catálogo de las Plantas Vasculares de Bolivia (Borsch et al., in press
), Flora of East Tropical Africa (Townsend, 1985
), Flora of Madagascar (Cavaco, 1954
), Flora of North America (Robertson and Clemants, 2003
), the conspectus of Australian Gomphrena (Palmer, 1998
), and a list of accepted names and synonyms prepared by Steve Clemants (Brooklyn Botanical Garden, unpublished data). Any species name in dispute was included in our data tables if numerous recent floras used the name. Specimens from species no longer recognized as valid are listed with their accepted synonyms in Appendices S1–S3 (see Supplemental Data with the online version of this article).
RESULTS
We examined 75 of the 77 recognized genera of the Amaranthaceae for carbon isotope ratio, often assaying the majority if not all species within a genus. The genera not examined because of a lack of available material were the monotypic genera Pseudosericocoma and Hebanthodes Pedersen (close to Hebanthe and probably C3). Genera examined here that have been recognized since Townsend (1993)
include Hebanthe, which forms a separate lineage within Gomphrenoideae (Müller and Borsch, 2005a
; I. Sánchez-del Pino and T. Motley, New York Botanical Garden, with T. Borsch, unpublished data); Lecosia, a Brazilian genus recognized by Pedersen (2000)
; Pedersenia, which constitutes an isolated lineage in Gomphrenoideae (T. Borsch lab, unpublished data; I. Sánchez-del Pino, T. Motley, and T. Borsch, unpublished data.); and Quaternella and Xerosiphon (Pedersen, 1990
). In total, we examined 607 species in the 77 genera listed in Table 1.
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and –21, which might indicate the presence of C4-like C3–C4 intermediate species (Sage, 2004
). The frequency distribution of isotope values of C3 and C4 species in Aerva and Gomphrena was similar to the frequency distribution of all C3 and C4 species in the study, indicating no trend toward an intermediate C3–C4 physiology (compare Figs. 1 and 2). By contrast, five species in Alternanthera had isotope values between –21.5 and –23.1, a range that corresponded to the upper fringe of all the C3 species in the study. An isotope value above –24 indicates either high water use efficiency or the potential for PEP carboxylase engagement in C3–C4 intermediacy (Farquhar et al., 1989
; Monson and Rawsthorne, 2000
). All three Alternanthera species previously shown to be C3–C4 intermediates (Al. crucis, Al. ficoidea, Al. tenella; Rajendrudu et al., 1986
; Rajendrudu and Das, 1990
; Fernandez et al., 1999
) had C3-like carbon isotopic values that averaged –28 (Table 2).
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) occurs in the Argentinian and Bolivian Andes at 3800 to 4600 m a.s.l. (Pedersen, 1990
; Borsch et al., in press
). The 4600 m collection of G. meyeniana examined here (Solomon, Stein and Uehlig 11794 from Valle del Zongo in Bolivia) is the highest-elevation C4 eudicot known in the world. The altitude record reported for any confirmed C4 species worldwide is 4800 m for the grass species Muhlenbergia peruviana (Ruthsatz and Hoffmann, 1984
). This species and G. meyeniana are the only known C4 plants above 4500 m in the western hemisphere. In the eastern hemisphere, the chenopod Salsola monoptera and the grass Orinus thoroldii are the only putative C4 species reported above 4500 m; both occur on the Tibetan Plateau (Wang, 2003
). Gomphrena umbellata (–12.9) and Am. peruvianus (–13.8) occur from 3700 to 4300 m in the central Andes of Bolivia and Argentina (Pedersen, 1990
; Borsch et al., in press
). Gomphrena meyeniana and Al. peruvianus have a typical alpine plant morphology, with small leaves tightly clustered on a thick root stock, whereas G. umbellata is an annual growing in dry sand fields. A fourth high-elevation C4 species that we noted is Al. microphylla (–12.4), which grows up to 4000 m a.s.l. in dry chaparral vegetation of the central Andes (Beck et al., 2001
; Borsch et al., in press
). A C3 species of Alternanthera also occurs in the Peruvian Andes above 4000 m a.s.l. (Al. lupulina, –27.4). These two Alternanthera species have a similar growth form and would be ideal for comparing C3 and C4 photosynthetic performance at high elevation. Parsimony analysis of combined matK/trnK sequences yielded 809 shortest trees of 2617 steps (CI = 0.620, RC = 0.466). The majority rule strict consensus is shown in Fig. 3, and one of the shortest trees is in Fig. 4. In Amaranthaceae, the basal grade consists of Bosea, followed by Charpentiera. The additional major lineages correspond to the tribe Celosieae, the Amaranthoid clade (Amaranthus and relatives), Psilotrichum ferrugineum and Allmaniopsis in isolated positions, the Aervoid clade (Aerva and relatives), and the Achyranthoid clade (containing mostly paleotropical genera). The largely neotropical subfamily Gomphrenoideae appears with the lineages of Iresine, Alternanthera, Tidestromia, Pedersenia, and Pseudoplantago in a polytomy with a well-supported clade comprising Blutaparon (C4), Froelichia (C4), Gomphrena (C4), Guilleminea (C4), Hebanthe (C3), Pfaffia (C3), and the C3 genus Xerosiphon (Fig. 3).
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Recent molecular studies have provided novel insights into phylogenetic relationships within the Amaranthaceae (Kadereit et al., 2003
; Pratt, 2003
; Müller and Borsch, 2005a
, b
). Here, we analyzed the matK/trnK sequences from Müller and Borsch (2005a, b), matK/trnK data from Iresine (T. Borsch et al., unpublished data) and several new matK/trnK sequences from Aerva, Alternanthera, and Amaranthus species to generate a more complete picture of relationships between C3 and C4 taxa within the Amaranthaceae (Figs. 3, 4). The topology of our matK/trnK tree is congruent with the trees found by Müller and Borsch (2005a, b); however, some nodes that were weakly supported in their analyses (e.g., Deeringia as sister to the remainder of Celosioid genera, and some deep nodes in Gomphrenoideae) were not resolved with statistical support when more taxa were added in this study (shown as polytomies in the majority rule consensus of Fig. 3).
Five different lineages with C4 photosynthesis are indicated. The first is the C4-only genus Amaranthus, which is depicted to be monophyletic within a monophyletic Amaranthoid lineage (Figs. 3, 4). Our addition of the genus Pleuropterantha shows that this drought-adapted tropical herb from Africa is sister to Amaranthus rather than to Chamissoa (a genus of woody shrubs and lianas of wet forests in the neotropics) as found in the previous phylogenetic analyses by Müller and Borsch (2005a, b). This finding is consistent with hypotheses that C4 photosynthesis evolved in dry regions (Sage, 2004
) and suggests that closer phylogenetic and ecophysiological examination of Amaranthus, Pleuropterantha, and putative relatives such as Digeria may provide clues to the origin of C4 photosynthesis in this clade.
The second C4 group is found in the aervoids and is constituted by a lineage of Aerva javanica and closely related species that appear sister to the herbaceous genus Nothosaerva. This study shows that most C3 species of Aerva occur in a different clade that is sister to Ptilotus. Aerva is therefore determined to be polyphyletic. This possibility was indicated by the respective positions of Ae. javanica and Ae. leucura in the analyses of Müller and Borsch (2005a, b). In a recent analysis of Aerva, Thiv et al. (2006)
also found two major clades in the genus. However, because Aerva was rooted with Ptilotus in their study, its polyphyly was not evident. One branch of Aerva, termed clade B by Thiv et al. (2006)
, is completely C3, with species Ae. coriacea, Ae. congesta, Ae. lanata, Ae. leucura, Ae. sanguinolenta, and Ae. triangularifolia. The C4 species of Aerva are segregated into a separate clade, along with the xerophytic C3 species Ae. artemisoides, Ae. microphylla, and Ae. revoluta (Thiv et al., 2006
). These C3 species should be close to the ancestor of the C4 species and thus may reveal insights into the evolution of C4 photosynthesis in Aerva.
All remaining C4 groups of Amaranthaceae are in the largely new world subfamily Gomphrenoideae, which is monophyletic (Müller and Borsch, 2005a
; I. Sánchez-del Pino, unpublished data). This third and most speciose C4 clade of Amaranthaceae comprises the genera Froelichia, Guilleminea, Blutaparon, C4Gomphrena (Fig. 3), and most likely also Gossypianthus and Lithophila. The latter two are not included in the phylogenetic analysis in this study, but pollen and morphological evidence strongly indicates that these two groups are members of this C4 clade (Borsch, 1998
). Lithophila also shares many morphological characters with Blutaparon (Eliasson, 1988
). Gomphrena has been suggested to be polyphyletic based on pollen (Borsch, 1998
) and sequence data (Kadereit et al., 2003
; Müller and Borsch, 2005a
). Notably, the C3 species of Gomphrena are unrelated to the core of the genus Gomphrena, which appears to be strictly C4 (Fig. 3). Our data support the view of Pedersen (1990)
that the C3 species formerly classified as G. angustifolia and G. aphyllus should be classified as members of the genus Xerosiphon. Species of Xerosiphon have metareticulate pollen with reduced tecta similar to C4Gomphrena species. By contrast, the C3 species classified as G. mandonii and G. elegans have metareticulate pollen with complete tecta as occurs in Pfaffia (Borsch, 1998
; T. Borsch lab, unpublished data). In the molecular tree, the respective C3Gomphrena species also appear as close relatives to Pfaffia and should eventually be reclassified within Pfaffia or a closely related genus.
The C3 genus Froelichiella has yet to be included in any molecular phylogenetic analysis. Eliasson (1988)
has pointed out that among Gomphrenoideae, Froelichiella is closest to Froelichia, indicating that it may be the nearest living C3 relative of the C4 lineage. There are notable differences between Froelichiella and Froelichia, however. For example, in Froelichiella the tepals are almost free to the base, the stigma is multilobate, and pseudostaminodia are distinct. Pollen morphology of Froelichiella is of the Gomphrena type (Borsch, 1998
) but has details very close to Xerosiphon (T. Borsch lab, unpublished data). A phylogenetic position for Froelichiella that is either sister to or diverging near Xerosiphon is thus hypothesized.
The fourth postulated C4 lineage is constituted by the monophyletic genus Tidestromia, which has a center of diversity in gypsum soils in Mexico and the United States (Sánchez-del Pino and Flores Olvera, 2006
). This is a small genus with eight C4 species. Current phylogenetic hypotheses raise the possibility of either Alternanthera and Tidestromia being sister groups (rbcL sequence data, Kadereit et al., 2003
; trnL-F sequence data, I. Sánchez-del Pino, unpublished data) or Pedersenia and Alternanthera being sister groups (rpl16 sequence data, rpl16+trnLF sequence data combined, I. Sánchez-del Pino, unpublished data). However, statistical support for either hypothesis is weak, and matK/trnK data of this study (Fig. 3) depict Alternanthera, Pedersenia, and Tidestromia in a polytomy. The addition of Al. altacruzensis, Al. flavescens, and Al. microphylla to the matK/trnK data set in this study indicates that C4 photosynthesis in Alternanthera arose in a terminal clade of the genus, well after the diversification of major Alternanthera lineages. Alternanthera therefore is the fifth independent C4 lineage in Amaranthaceae.
Recent work using trnLF and rpl16 sequence data and more species indicates Alternanthera to be monophyletic (I. Sánchez-del Pino, unpublished data) and also suggests C3 photosynthesis to be the plesiomorphic condition in the genus. The C4 and C3–C4 intermediate species of Alternanthera appear to occur in one subclade of procumbent herbs that form a terminal clade relative to the C3Alternanthera species. These species are largely South American, in contrast to Tidestromia, which is centered in northern Mexico and the southwestern USA. This difference in the center of diversity between the C4Alternanthera species and Tidestromia also supports the hypothesis that C4 photosynthesis independently arose in these two genera. A distinct origin of C4 photosynthesis in Alternanthera is also supported by the occurrence of three species in the genus with biochemical and anatomical traits that are intermediate between the full C3 and C4 conditions (Fernandez et al., 1999
). The exact phylogenetic position of these intermediates, however, is not currently known. Because Alternanthera is species rich compared to other genera with identified C3–C4 species, it may be an excellent system to study the evolution of the C4 pathway. A priority for future work with Alternanthera should be clarification of the phylogenetic positions of the C3, C3–C4, and C4 species.
C3–C4 intermediate species are classified into two functionally distinct groups. The first group comprises intermediate species that have an efficient system to recapture photorespired CO2. This occurs by localizing the photorespiratory enzyme glycine decarboxylase in the bundle sheath tissue and transporting all photorespiratory metabolites formed in a leaf to this compartment for decarboxylation (Monson and Rawsthorne, 2000
; Sage, 2004
). The released CO2 accumulates in the bundle sheath tissue and is refixed by Rubisco present in these cells. These species are termed type I C3–C4 intermediates (Edwards and Ku, 1987
). Type I intermediates have a typical C3 isotopic signature because all CO2 fixation occurs via Rubisco and the 13C ratio reflects isotopic discrimination by Rubisco. Thus, isotopic screens cannot identify type I intermediates, which include the three Alternanthera intermediates previously identified by biochemical and anatomical studies (Rajendrudu et al., 1986
; Rajendrudu and Das, 1990
; Devi and Raghavendra, 1993
). The second group (type II intermediates sensu Edwards and Ku, 1987
) has enhanced activity of PEP carboxylase and a limited C4 cycle. In type II intermediates, initial fixation of CO2 by PEP carboxylase increases the 13C ratio toward C4-like values; however, to rise above the –21 threshold that excludes C3 species, the activity of PEP carboxylase has to be substantially enhanced, typically above 50% of the activity of Rubisco (Monson et al., 1988
; Monson and Rawsthorne, 2000
). We did not identify any species with 13C ratios between –17 to –21 that are strong indicators of type II intermediacy; however, we did identify a number of Alternanthera species (Al. dolichocephala, Al. echinocephala, Al. eupatoroides, Al. snodgrassii, and Al. spinosa) with 13C values that stood out because they were on the upper fringe of the C3 distribution. These species would be excellent candidates to examine for type II intermediacy. Alternatively, these species may have low stomatal conductances often seen in xeric species; low stomatal conductance relative to photosynthetic capacity generally explains high isotope ratios in C3 species (Farquhar et al., 1989
).
This survey identified 233 C4 species of the 607 examined in the Amaranthaceae. With perhaps two dozen C4 species not examined in the survey, we estimate there are about 250 C4 species in the Amaranthaceae or about 28% of the 900 species estimated to occur in the family (Townsend, 1993
). This value is identical to the 250 C4 species previously estimated by Sage et al. (1999)
. Sage et al. (1999)
listed Achyranthes and Celosia as having C4 species, based on earlier reports of Kranz anatomy. Our results show no evidence of C4 photosynthesis in either Achyranthes or Celosia, although enlarged bundle sheath cells may indicate C3–C4 intermediacy.
In conclusion, we provide the first comprehensive survey of the distribution of the photosynthetic pathways within a large eudicot family that evolved C4 photosynthesis multiple times. By clarifying which species are C3, in addition to which are C4, this survey provides important information for a range of disciplines for which the photosynthetic pathway has important consequences. Evolutionary studies will benefit by having the proper placement of the C4 pathway in a phylogenetic sequence. With the development of fine scale phylogenies, our results can be used to identify closely related C3 and C4 species, which would then facilitate studies on the evolutionary changes involved in C4 plant evolution. By knowing with certainty whether a species is C3 or C4, ecologists will be able to identify the ecological significance of a photosynthetic pathway in a given flora and within a vegetation community. In combination with evolutionary studies, ecological research with closely related C3 and C4 species could identify in greater detail the ecological conditions favoring the rise of C4 photosynthesis. The current understanding is that C4 species arose in hot, arid or saline environments, but no study has clearly documented the local ecological conditions where any specific C4 lineage first appeared; hence, the generalization remains untested. Our survey has also identified species of interest to physiological ecologists. For example, the identification of C3 and C4Alternanthera species from high elevations and of Gomphrena meyeniana as the world's highest-elevation C4 eudicot provides a robust system for examining adaptation of the C4 pathway for cold climates that are markedly different from the hot environments where the pathway is believed to have first evolved.
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1 The authors thank M. Nee and N. Tarnowsky of the New York Botanical Garden, J. Solomon of the Missouri Botanical Garden, S. Atkins and K. Vollesen of Kew Gardens, and E. Wood of the Arnold Arboretum and Grey Herbarium for assisting in the access to herbarium materials. S. Clemants of the Brooklyn Botanical Garden kindly provided pre-published species lists of many Amaranthaceae genera. M. Frohlich of the British Museum of Natural History provided specimens from the British Museum Herbarium. L. Craven of the Australian National Herbarium and D. Kubien of the University of New Brunswick provided specimens of Australian Gomphrena. The authors are grateful to K. Müller (Bonn) for providing an unpublished trnK/matK sequence for Amaranthus praetermissus, and to G. Kadereit (Mainz) and K. Wilhelm (Oldenburg) for valuable comments on an earlier version of the manuscript. Funding was provided by grants BO 1815/1–1 and 1–3 and a Heisenberg fellowship from the Deutsche Forschungsgemeinschaft (DFG) to T.B. and grant OGP-0154273 from the Natural Science and Engineering Council of Canada to R.F.S. 
2 Author for correspondence (e-mail: R.sage{at}utoronto.ca
)
6 Current address: Plant Biodiversity and Evolution Group and Botanical Garden, Carl von Ossietzky Universität Oldenburg, 26111 Oldenburg, Germany
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