Molecular phylogeny of Camphorosmeae (Camphorosmoideae, Chenopodiaceae): Implications for biogeography, evolution of C₄‐photosynthesis and taxonomy

Abstract

Camphorosmeae constitute a species‐rich tribe of Chenopodiaceae‐Camphorosmoideae that consists mostly of subshrubs and annuals, distributed in steppes and semi‐deserts of Australia, Eurasia, North Africa, southern Africa and North America. We study (1) the relationships of Camphorosmeae to major lineages of the closely related Salsoloideae and (2) the diversification of the tribe with focus on the non‐Australian members using sequence variation of five different markers (rbcL gene, ndhF gene, atpB‐rbcL spacer, psbB‐psbH spacer, ITS) and morphological characters. The cpDNA analyses revealed six early‐branching lineages in Camphorosmoideae/Salsoloideae (Camphorosmeae, Salsoleae s.str., Caroxyloneae, Salsola kali clade, Nanophyton clade, Salsola genistoides clade) and supported partly (ndhF and atpB‐rbcL spacer) the sister‐group relationship of Camphorosmeae and all Salsolean clades. The distinctness of Camphorosmeae and Salsoleae s.l. is further supported by seed, stigma and pollen morphology. Molecular clock estimates point to an earlier radiation in Salsoleae s.l. (Early to Middle Oligocene) than in Camphorosmeae (Early Miocene). In Salsoleae s.l. early radiation might have been enhanced by multiple evolution of C4‐photosynthesis which facilitated the spread into drier habitats of Eurasia. In Camphorosmeae, C4‐photosynthesis likely evolved two times, probably in the Middle Miocene. During the Miocene Camphorosmeae spread from Eurasia to Australia, North America and at least two times to South Africa. Only the Australian lineage diversified, the others remained species‐poor. The molecular trees congruently resolve three major clades of unclear relationship within Camphorosmeae, Chenolea clade (five widely disjunct and morphologically divergent C3‐species, possibly remnants of old lineages), Sclerolaena clade (ca. 150 C3‐species from Central Asia [3 spp.] and Australia [147 spp.], probably the results of a rapid radiation during the Pliocene) and Bassia/Camphorosma clade (ca. 23 C4‐species and one C3/C4‐intermediate which are widely distributed in Eurasia and southern Africa). The phylogenies show the artificial state of the current generic and subtribal classifications of Eurasian, North American and South African Camphorosmeae. All non‐monotypic genera except Camphorosma and Neokochia were found to be polyphyletic. A revised classification of the tribe is proposed including reinstatement of the newly defined subfamily Camphorosmoideae, description of the new genera Spirobassia (1 sp.), Eokochia (1 sp.), Grubovia (3 spp.) and Sedobassia (1 sp.), and several new combinations and synonymizations.

Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis

“…8), which is consistent with this hypothesis. Similar positioning of S. webbii and S. genistoides has been previously suggested by Kadereit et al (2003) and Kadereit and Freitag (2011), but with many fewer Salsoleae species sampled and with some variation in their precise position depending on the analysis. Here strong support is found for these species forming a grade at the base of the Salsoleae s.s.…”

“…Among eudicot families, it is well established that family Chenopodiaceae has the largest number of C 4 species (Akhani et al, 1997; Kadereit and Freitag, 2011; Sage et al, 2012), and also the greatest diversity in C 4 -type leaf anatomy, with eight main structural types (Carolin et al, 1975; Edwards and Voznesenskaya, 2011), and up to 16 forms considering all differences (Kadereit et al, 2003). This includes the occurrence of Kranz anatomy around individual veins as well as Kranz anatomy with a concentric dual layer of cells surrounding all the veins in the leaf, and two structural forms of C 4 occurring in individual cells without Kranz anatomy.…”

“…This includes the occurrence of Kranz anatomy around individual veins as well as Kranz anatomy with a concentric dual layer of cells surrounding all the veins in the leaf, and two structural forms of C 4 occurring in individual cells without Kranz anatomy. Currently, 10 C 4 lineages have been recognized in Chenopodiaceae (Kadereit and Freitag, 2011; Sage et al, 2012). …”

“…However, despite the diversity of C 4 in family Chenopodiaceae, to date only one species, Salsola arbusculiformis in subfamily Salsoloideae, has been structurally and functionally characterized to be a C 3 –C 4 intermediate (Voznesenskaya et al, 2001). Another species, Sedobassia sedoides in subfamily Camphorosmoideae, was recently suggested to be an intermediate based on anatomical features (Kadereit and Freitag, 2011); and shown to function as an intermediate based on gas exchange analysis and immunolocalization of glycine decarboxylase (GDC) (NKK, EVV, and GEE, unpublished data).…”

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

“…The analysed dataset consisted of 95 C 3 and 84 C 4 species (Table S1). Most of the included sequences came from four studies [19], [28], [29], [30] and evenly represented all main lineages within the family (Fig. 1).…”