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Physiology and Biochemistry |
2Department of Plant Physiology, Urals State University, Lenin Avenue 51, 620083 Ekaterinburg, Russia 3School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 USA 4Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602 USA
Received for publication May 23, 2000. Accepted for publication November 21, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: C3 and C4 photosynthesis • Chenopodiaceae • evolution • ITS sequences • leaf anatomy • phylogeny • Salsola
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Shomer-Ilan, Nissenbaum, and Waisel, 1981
; Zalenskii and Glagoleva, 1981
; Voznesenskaya and Gamaley, 1986
; Pyankov et al., 1992, 1997
; Akhani, Trimborn, and Ziegler, 1997
). Among the C4 species, variation also occurs in the types of Kranz anatomy (details in Carolin, Jacobs, and Vesk, 1975
) and in the biochemical subtypes of the C4 pathway. This variation is generally correlated, such that species with Atriplicoid and Suaedoid types of Kranz anatomy have the NAD-ME C4 photosynthetic subtype, and species with Kochioid anatomy have the NADP-ME C4 photosynthetic subtype. Only the Salsoloid anatomical group has both NAD-ME and NADP-ME subtypes (Zalenskii and Glagoleva, 1981
; Pyankov and Vakhrusheva, 1989
; Gamaley et al., 1992
; Pyankov et al., 1992, 1997
; Fisher et al., 1997
). The general correspondence of anatomical type and tribal limits inferred from morphology suggests multiple evolutionary lineages with C4 photosynthesis (Pyankov, 1991
; Gamaley et al., 1992
; Pyankov et al., 1992, 1997
), as in the Poaceae (Hattersley and Watson, 1992
; Kellogg, 1999
).
Diversity in habitats, life forms, and photosynthetic characters in assimilation organs is particularly complex in Salsola, a genus of 100 (Freitag, 1997
) to nearly 200 (Botschantzev, 1967, 1968, 1969, 1979
) species, and related genera in tribe Salsoleae. Two anatomical types, Salsoloid and Sympegmoid (Carolin, Jacobs, and Vesk, 1975
), occur in leaves of species of Salsola. Salsoloid type leaves are characterized by two continuous layers of chlorenchymatous cells (a layer of palisade mesophyll cells and an inner layer of very distinctive Kranz type bundle cells) on the periphery and water-storage parenchyma in the center. The main vascular bundle occupies the central position in the leaf, and only the small, peripheral vascular bundles are in contact with the chlorenchyma. Some species with Salsoloid anatomy have NAD-ME C4 photosynthesis whereas others have the NADP-ME C4 subtype (Zalenskii and Glagoleva, 1981
; Pyankov and Vakhrusheva, 1989
; Pyankov et al., 1992, 1997
). Sympegmoid type leaves are characterized by having two or three layers of palisade cells and a discontinuous layer of indistinctive bundle sheath cells (typically non-Kranz) around water-storage tissue (Carolin, Jacobs, and Vesk, 1975
; Pyankov et al., 1997
). Plants with Sympegmoid anatomy have C3-like 13C/12C carbon discrimination values (Akhani, Trimborn, and Ziegler, 1997
; Pyankov et al., 1997
). Variation also occurs in structural and biochemical features in cotyledons (Pyankov et al., 1998
; Pyankov, Artyusheva, and Edwards, 1999
). Two non-Kranz types, isopalisade and dorsoventral, and two types of Kranz anatomy, Atriplicoid and Salsoloid, are found in Salsola cotyledons (Butnik, 1979
; Butnik et al., 1991
; Pyankov et al., 1998
; Pyankov, Artyusheva, and Edwards, 1999
). Finally, Kranz-type cotyledons and leaves may or may not contain a hypodermis. The result is a number of unique combinations of structural and biochemical photosynthetic types in leaves and cotyledons in species of Salsoleae.
Kellogg (1999)
demonstrated multiple origins of C4 photosynthesis in each of the families Poaceae, Cyperaceae, Asteraceae, and Zygophyllaceae. Multiple origins of C4 photosynthesis appear likely within Chenopodiaceae as well, and the diversity of photosynthetic types and anatomical structures in Salsoleae suggests a dynamic pattern of photosynthetic evolution within this single tribe. Despite extensive systematic treatments of Salsola and relatives (e.g., Botschantzev, 1969
; Freitag, 1997
), the number of species and species groups remains uncertain, and no explicit phylogeny of Salsoleae has been presented to place the photosynthetic diversity in a historical context.
The internal transcribed spacer (ITS) region of 18S–26S nuclear ribosomal DNA (nrDNA) has proven to be a useful source of characters for phylogenetic relationships within genera and among closely related genera in many angiosperm families (e.g., Baldwin et al., 1995
). We therefore used ITS sequences to reconstruct the phylogeny of tribe Salsoleae in order to address questions about the origin and evolution of the C4 syndrome in Salsola and related genera.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Tzvelev, 1993
; Freitag, 1997
). Other genera of Salsoleae, considered by Botschantzev (1969)
to be derived from Salsola, were also included. Four species from outside Salsoleae (Camphorosma lessingii, Kochia prostrata, K. scoparia, and Atriplex spongiosa) were included as outgroups (Table 1).
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) and a microprep procedure (Cullings, 1992
). Both fresh leaves from living plants and dried leaves taken from herbarium specimens served as sources of DNA. Fresh leaves were desiccated on silica gel for 1 wk prior to DNA extraction.
DNA amplification and sequencing
The ITS regions were amplified using the primer combination N-nc18S10/C26A (Wen and Zimmer, 1996
). Automated sequencing was performed using these same primers, following the general methods outlined by Soltis and Soltis (1997)
and the Big Dye Deoxy Terminator (Applied Biosystems, Inc., Foster City, California, USA) with an ABI 377 automated DNA sequencer.
Alignment and phylogenetic analysis
ITS sequences were deposited in GenBank (accession numbers AF318619–AF318656). ITS sequences were aligned manually by sequential pairwise comparison. Gaps of one or more nucleotide positions were inserted to align the sequences; gaps were scored as missing data in phylogenetic analyses. Parsimony analyses were conducted using PAUP* 4.0 (Swofford, 1998
) on Macintosh Power PC computers. Heuristic searches involved 500 replicates with random taxon addition and nearest neighbor interchange (NNI) branch swapping, saving ten trees per replicate. These 840 trees (of lengths 861–882) served as starting trees for further analyses using tree bisection reconnection (TBR) branch swapping and saving all most parsimonious trees. Bootstrap analysis (Felsenstein, 1985
) with 500 replicates, each with random taxon addition and TBR branch swapping and saving ten trees per replicate, was used to assess support for clades. Species from tribe Camphorosmeae (Camphorosma lessingii, Kochia scoparia, and K. prostrata) and tribe Atripliceae (Atriplex spongiosa) were used as outgroups.
Reconstructing the history of photosynthetic, anatomical, and distributional characters
To investigate the evolutionary history of photosynthetic and anatomical characters in both cotyledons and leaves of Salsoleae, we mapped the photosynthetic and anatomical types on the strict consensus tree using parsimony optimization and the TRACE option of MacClade version 3.04 (Maddison and Maddison, 1992
). Photosynthesis in cotyledons was scored as C3 (0), C4-NAD-ME (1), and C4-NADP-ME (2). Anatomy in cotyledons was scored as dorsoventral (DV; 0), isopalisade (IP; 1), Atriplicoid with hypodermis (ATR+H; 2), Salsoloid with hypodermis (SALS+H; 3), and Salsoloid without hypodermis (SALS–H; 4). Photosynthesis in leaves was scored as C3 (0), C4-NAD-ME (1), and C4-NADP-ME (2). Anatomy in leaves was scored as Salsoloid with hypodermis (SALS+H; 0), Salsoloid without hypodermis (SALS–H; 1), Sympegmoid (SYMP; 2), Atriplicoid with hypodermis (ATR+H; 3), and Kochioid (KOCH; 4). All photosynthetic and anatomical characters were treated as unordered, and data used in reconstructions are from Butnik (1979)
, Gamaley et al. (1992)
, and Pyankov et al. (1997, 1998
, unpublished data).
To evaluate Botschantzev's (1969)
hypotheses of the location of origin and subsequent diversification and migration of Salsola, we plotted the geographic distributions using the TRACE option of MacClade and the strict consensus tree. Geographic distributions for species of Salsoleae and outgroups included in the analysis were taken from Botschantzev (1969, 1976, 1979)
. Nine geographic areas were identified and coded as southern Africa (0), southwestern Africa (1), northern Africa (2), Middle East (3), central Asia—large (4), central Asia—small (5), Mongolia (6), China (7), and Europe (8). The geographic designations for each species are given in Table 1; several species were coded as polymorphic.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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50%. The outgroups K. prostrata, K. scoparia, and C. lessingii are NADP-ME type C4 species. The clade of 18 species of Salsoleae includes 14 species with NAD-ME C4 photosynthesis and four species with C3 or C3–C4 photosynthesis, in leaves. The second subclade (with 99% bootstrap support) contains the remaining 16 species of Salsoleae, all but two (with C3 or C3–C4-like photosynthesis) of which have NADP-ME C4 photosynthesis in leaves.
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Both the NAD-ME and NADP-ME clades contain species assigned to other genera that were considered "derivatives" of Salsola by Botschantzev (1969)
. In the NAD-ME clade are Climacoptera lanata and Halocharis gossypina. The NADP-ME clade includes Halothamnus subaphyllus, Haloxylon ammodendron, H. persicum, and Girgensohnia oppositiflora.
Character reconstructions
Parsimony reconstructions of photosynthetic and anatomical characters show dynamic patterns of evolution in features of both cotyledons and leaves. The reconstruction of photosynthetic type in mature leaves on all trees supports the split into two groups in Salsoleae (the NAD-ME and NADP-ME lineages) (Fig. 2). Although the ancestral nodes are equivocal, reversion to C3 (or C3-like) photosynthesis in leaves occurred once in each lineage, in the ancestor of S. drobovii, S. laricifolia, S. oreophila, and S. botschantzevii in the NAD-ME lineage and in the ancestor of S. montana and S. arbusculiformis in the NADP-ME lineage. The ancestral leaf anatomy in Salsoleae was reconstructed on all trees as Salsoloid without hypodermis (SALS–H) (Fig. 3). All other types apparently evolved from SALS–H. The addition of hypodermis (SALS+H) and Sympegmoid anatomy both arose independently in the NAD-ME and NADP-ME lineages from SALS–H ancestors.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Pyankov, unpublished data). The ITS phylogeny also recovered groups of species that generally correspond to the sections and subsections of Salsola sensu Botschantzev (1969, 1976, 1979)
. The phylogeny also supports many of Botschantzev's (1969)
hypotheses regarding the derivation of taxonomically recognized genera from within Salsola (e.g., Halothamnus, Haloxylon, Girgensohnia, Climacoptera, and Halocharis).
Phylogeny: Comparisons with taxonomy and photosynthetic data
NAD-ME lineage
This lineage includes representatives of five sections, Coccosalsola, Caroxylon, Malpigipila, Cardiandra, and Belanthera; the latter three sections were considered by Botschantzev (1969)
to have had a common origin from section Caroxylon, and other authors agreed regarding the morphological similarity and apparent close relationships of all of these sections except Coccosalsola (Tzvelev, 1993
; Freitag, 1997
).
Sister to the NAD-ME lineage are two of the outgroups, Kochia and Camphorosma, but this relationship is only weakly supported (bootstrap value <50%). The nonmonophyly of Salsoleae found here may be an artifact of the sampling used in this analysis or it may reflect true relationships in Chenopodiaceae. Ongoing revisionary work in Salsoleae is consistent with the hypothesis that Salsola is polyphyletic (H. Freitag, personal communication). Recent phylogenetic analyses have likewise demonstrated that Chenopodiaceae are not monophyletic, with genera of Amaranthaceae intermingled with those of Chenopodiaceae (e.g., Manhart and Rettig, 1994
; Downie, Katz-Downie, and Cho, 1997
). Further study is needed to test the monophyly of Salsola and of Salsoleae, to infer relationships among genera currently classified in Chenopodiaceae and Amaranthaceae, and to assess the evolution of photosynthetic characters in the Chenopodiaceae/Amaranthaceae clade.
Within the NAD-ME lineage of Salsoleae are two main clades. One of these consists of Climacoptera lanata as sister to a clade of species from sections Cardiandra (S. leptoclada), Malpigipila (S. gemmascens and S. passerina), and Caroxylon (six species). Three small clades within this clade received moderate to high bootstrap support: the sister relationship of S. gemmascens and S. passerina (98%), the Caroxylon-1 clade (S. incanescens, S. laricina, and S. dendroides; 81%), and the Caroxylon-2 clade (S. cyclophylla, S. albisepala, and S. albida; 82%). The Caroxylon-2 clade largely corresponds to Botschantzev's (1969)
section Caroxylon subsection Caroxylon, although S. angolensis (which appears in the NADP-ME lineage) and S. dendroides (which is part of Caroxylon-1) are not included in the clade. Salsola laricina and S. incanescens belong to Botschantzev's (1969, 1979)
subsection Vermiculatae and were considered to be derivatives of subsection Caroxylon. Freitag (1997)
placed S. dendroides in subsection Vermiculatae as well, because it shares a hypogynous disc, linear filaments, and other characters with species in that subsection; this relationship to other species classified as subsection Vermiculatae is supported by the ITS phylogeny. All representatives of section Caroxylon examined have a similar type of Kranz anatomy in leaves (SALS+H) and cotyledons (ATR+H) (Table 1).
The Malpigipila clade (the sister pair of S. gemmascens and S. passerina) and S. leptoclada from section Cardiandra share similar features of photosynthesis in leaves and cotyledons. The cotyledons have C3 type photosynthesis with dorsoventral mesophyll structure, and the leaves have C4 NAD-ME type photosynthesis with Salsoloid Kranz anatomy without a hypodermis. Botschantzev (1969)
proposed that section Malpigipila originated from section Caroxylon and that section Cardiandra is derived from Malpigipila. Although the relationships of these species are not well supported in the ITS phylogeny, the positions of species classified in sections Cardiandra and Malpigipila do not support Botschantzev's hypothesis.
The second large clade of the NAD-ME lineage includes Halocharis gossypina as sister to a clade of species from section Belanthera and section Coccosalsola subsection Arbuscula (with 94% bootstrap support). Salsola aucheri, S. gossypina, and S. kopetdaghensis of section Belanthera are successive sisters to a clade (91% bootstrap support) containing some, but not all, of Botschantzev's (1969)
section Coccosalsola subsection Arbuscula. Included in this clade are S. drobovii, S. laricifolia, S. oreophila, and S. botschantzevii. Salsola montana, S. arbusculiformis, S. arbuscula, S. chiwensis, and S. richteri, all of which were also placed in subsection Arbuscula by Botschantzev, occur in the NADP-ME lineage. Botschantzev (1969)
and others (Tzvelev, 1993
; Freitag, 1997
) considered sect. Belanthera to be derived from section Caroxylon, but this relationship is not supported by the ITS phylogeny (Fig. 1). Instead, the ITS phylogeny indicates a common ancestor for the Belanthera + Coccosalsola clade and the clade composed of species from sections Caroxylon, Malpigipila, Cardiandra, and Coccosalsola. Climacoptera lanata and Halocharis gossypina were considered by Botschantzev (1969)
to be derived from section Belanthera. Given their phylogenetic position deep within Salsola, Climacoptera and Halocharis should be reclassified as species of Salsola. Salsola aucheri, S. gossypina, S. kopetdaghensis, and H. gossypina have the same photosynthetic structures and biochemistry as species of sections Malpigipila and Cardiandra (Table 1). Given the shared photosynthetic characteristics of most of the species in this clade, the common ancestor of the NAD-ME lineage had C3 photosynthesis and dorsoventral anatomy in cotyledons and NAD-ME C4 photosynthesis and SALS–H anatomy in leaves (Figs. 2–5). Species having C4 type cotyledons evolved from C3 in the NAD-ME lineage, but the results with species in the NADP-ME lineage are equivocal. However, the clade of S. drobovii, S. laricifolia, S. oreophila, and S. botschantzevii is characterized, in contrast, by leaves having Sympegmoid anatomy and C3 (or C3-like) photosynthesis based on carbon isotope composition (Butnik, 1979
; Pyankov et al., 1997
, unpublished data; see Table 1) and cotyledons having C3 type anatomy (S. drobovii, information not available on other species). These characteristics indicate a derivation of Sympegmoid anatomy and reversion to C3 photosynthesis in leaves in the common ancestor of this clade (Figs. 2, 3).
NADP-ME lineage
An independent evolutionary lineage with NADP-ME C4 photosynthesis is strongly supported by both ITS sequence analysis (Fig. 1) and physiological data (Table 1). All species belonging to this lineage have different photosynthetic features in the assimilating organs than those in the NAD-ME line. All but two of them (which are C3 or C3-like) have NADP-ME C4 photosynthesis in leaves; all have either NADP-ME C4 photosynthesis in cotyledons with Salsoloid anatomy or C3 photosynthesis with isopalisade mesophyll structure. Neither NAD-ME C4 photosynthesis nor Atriplicoid or dorsoventral mesophyll types were found in species of this lineage. The species in the NADP-ME lineage belong to section Coccosalsola subsections Arbuscula, Coccosalsola, and Genistoides sensu Botschantzev (1976
; equivalent to sections Arbuscula, Coccosalsola, and Genistoides sensu Freitag, 1997
). Five small, well-supported clades are present within the NADP-ME lineage; relationships among these clades are completely resolved in all of the shortest trees, but they are not supported by bootstrap values 50%. These five clades within the NADP-ME lineage will be discussed below.
1) Sympegmoid (SYMP) clade—Two species in our analysis, S. arbusculiformis and S. montana, form a sister pair in the NADP-ME lineage, with Sympegmoid anatomy. Although S. arbusculiformis has C3-like 13C/12C carbon discrimination values, it resembles C4 plants in its Kranz-like cells with many chloroplasts, indicative of a C3–C4 intermediate (Pyankov et al., 1997
). Carolin, Jacobs, and Vesk (1975)
suggested that Sympegmoid anatomy may have evolved from the Salsoloid type, a change that would require a reversion from C4 to C3 photosynthesis. The vasculature in the Sympegmoid type is very similar to that of Salsoloid Kranz anatomy, and it is unlike any other non-Kranz type in Chenopodiaceae. The presence of small vascular bundles just beneath the chlorenchymatous mesophyll further suggests a relationship with the Salsoloid type of Kranz anatomy. Sympegmoid leaves have three layers of chlorenchema cells, while Salsoloid leaves have two layers that surround a central bundle embedded in water storage tissue. Photosynthetically, Salsola species with the Sympegmoid structure belong to a group of plants classified as C3, or C3–C4 intermediate species, which may represent an intermediate stage of evolution from C3 to C4 or vice versa (Edwards and Ku, 1987
). The ITS phylogeny of Salsoleae suggests that species in the NADP-ME lineage with Sympegmoid anatomy (S. arbusculiformis and S. montana) evolved from Salsola species having C4 photosynthesis. Several species of Salsola with Sympegmoid anatomy occur in the Pamir and Tien-Shan mountains; many C4 Salsola species cannot survive in cooler conditions and may have disappeared during geological changes (Botschantzev, 1969
). However, a reversion from C4 to C3 photosynthesis in these cool habitats seems likely (Pyankov et al., 1997
) and is supported by the ITS phylogeny. Such a reversion from C4 to C3 photosynthesis has been inferred for Eragrostis walteri, the only species in Eragrostis that is not C4 (Ellis, 1984
).
As noted earlier, four species of the NAD-ME lineage (S. drobovii, S. laricifolia, S. oreophila, and S. botschantzevii) also have Sympegmoid anatomy and C3-like photosynthesis, and Botschantzev (1969)
placed these species, plus S. montana, S. arbusculiformis, S. arbuscula, S. chiwensis, and S. richteri, in section Coccosalsola subsection Arbuscula. However, reconstructions of anatomical and photosynthetic characters on the ITS tree show independent origins of Sympegmoid anatomy and reversions to C3 photosynthesis (Figs. 2, 3).
2) Haloxylon clade—The Haloxylon clade is sister to the Sympegmoid clade in all shortest trees and includes Haloxylon ammodendron, H. persicum, Girgensohnia oppositiflora, and Halothamnus subaphyllus. The members of this clade have isopalisade anatomy with C3 photosynthesis in cotyledons and Salsoloid Kranz anatomy, and except for H. subaphyllus, with hypodermis in green shoots/leaves. Botschantzev (1969, 1976)
viewed Haloxylon, a genus of large shrubs, to be derived from section Coccosalsola subsection Arbuscula, and Girgensohnia (which are annuals) to be derived from annuals in section Salsola. Instead, however, the ITS phylogeny supports a sister-group relationship between Haloxylon and Girgensohnia (with 85% bootstrap support), and this clade is not closely related to either the Arbuscula or Salsola clades of the NADP-ME lineage (see below). Halothamnus subaphyllus is the sister to the Haloxylon-Girgensohnia sister pair in all shortest trees, although this relationship does not receive bootstrap support 50%. Based on photosynthesis types in assimilation organs (Table 1), Halothamnus is similar to the "Haloxylon" type, i.e., C3 cotyledons with isopalisade mesophyll. Botschantzev (1969)
considered Halothamnus to share a common ancestor with Haloxylon, a relationship generally supported by the shortest ITS trees, with the inclusion of Girgensohnia as the sister to Haloxylon. Some differences between Halothamnus and Haloxylon exist in cotyledon size, morphology, and longevity: cotyledons in Haloxylon are small (0.5–1 cm) and short-lived (
2 wk), whereas in Halothamnus they are longer (up to 1.5–2 cm) and longer-lived (3–4 wk).
3) Foliosa clade—Salsola zygophylla and S. foliosa (the Foliosa clade) are the sister to the Sympegmoid + Haloxylon clade in all shortest trees, although bootstrap support for this relationship is <50%. These species are not part of the Arbuscula + Salsola clade (below), despite their biochemical and anatomical similarities (Table 1).
4) Arbuscula and Salsola clades—The Arbuscula and Salsola clades are sisters in all shortest trees (but with bootstrap support <50%) and contain species from section Coccosalsola subsection Arbuscula and section Salsola, respectively. The Arbuscula clade (S. arbuscula, S. richteri, S. chiwensis, and S. angolensis) and the Salsola clade (S. kali, S. paulsenii, and S. australis) are similar in photosynthesis type in leaves and cotyledons. The species of both clades have Salsoloid type Kranz anatomy and NADP-ME biochemistry in both cotyledons and leaves (Table 1). However, species of the Salsola clade lack hypodermal tissue in leaves, whereas hypodermis is present in species of the Arbuscula clade. The close relationships between these groups was also noted by Botschantzev (1969, 1976)
, who suggested a direct origin of section Salsola from subsection Arbuscula.
Evolutionary patterns in Salsoleae
Photosynthetic and anatomical characters have a dynamic history in Salsoleae, with C3 photosynthesis in cotyledons and leaves, the development of hypodermis in mature leaves, and Sympegmoid leaf anatomy evolving independently in the NAD-ME and NADP-ME lineages. Although its history is less clear, cotyledon anatomy is quite diverse, with five anatomical types described for the species of Salsoleae included in the analysis; at least a few of these types likely evolved multiple times in parallel in Salsoleae.
Botschantzev (1969)
proposed an elaborate hypothesis for the origin, diversification, and distribution of Salsoleae. He suggested that Salsoleae arose in Africa and subsequently dispersed to and diversified in the Middle East, central and eastern Asia, and Europe. Our reconstruction of geographic distributions contradicts this scenario. Instead, based on the species sampled, Salsoleae appear to have originated in central Asia, with more recent dispersal to Africa (independently for the ancestor of the S. albisepala-S. albida clade, S. zygophylla, and S. angolensis), to Mongolia (independently in the ancestor of S. gemmascens and S. passerina and in the broad-ranging S. laricifolia, S. arbuscula, S. paulsenii, S. foliosa, and H. ammodendron), and to Europe (e.g., S. kali) (Fig. 6). More species need to be collected from Africa for a more comprehensive evaluation of the origin of this tribe. In addition, the phylogenetic and biogeographical framework provided by this study should permit the development and testing of more informed hypotheses of the adaptations required for colonization and survival in the extremely harsh environments occupied by these plants.
Summary
This study demonstrates generally good agreement between clades inferred from phylogenetic analysis of ITS sequences (Fig. 1) and groups of species of Salsola based on morphological (e.g., Botschantzev, 1969, 1976
) and physiological data (Table 1). Reconstruction of photosynthetic characters on the ITS phylogeny of Salsoleae demonstrates separate NAD-ME and NADP-ME lineages. The existence of two lineages of C4 plants (NAD-ME vs. NADP-ME) in the tribe is further supported by analysis of a larger number of Salsola species based on structural and biochemical features of photosynthesis in leaves and cotyledons (Pyankov et al., 1997, 1998, 1999
, unpublished data; Pyankov, Artyushera, and Edwards, 1999
). The trees suggest a single origin of C4 photosynthesis in Salsoleae (rather than independent origins of the two types from C3 ancestors). It is thus possible that one type of C4 photosynthesis evolved first and the other was derived from it, but this hypothesis will need to be evaluated by analysis of a larger collection of species in Salsoleae and other genera of Chenopodiaceae and Amaranthaceae. The clades within the NAD-ME and NADP-ME lineages generally share similar biochemical and anatomical characters of both leaves and cotyledons, although reversion to C3 photosynthesis occurred in both clades. Reconstruction of geographic distributions suggests that Salsoleae originated and diversified in central Asia and subsequently dispersed to Africa, Europe, and Mongolia, in contrast to Botschantzev's (1969)
hypotheses of biogeography and radiation.
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FOOTNOTES |
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5 Author for reprint requests.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Artzichovskii V. M. 1928 Sexual growth and the development of its stem. Trudy po Prirladnoi Botanike, Genetike I Selekzii. 19 (in Russian)
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