Phylogeny of Salicornioideae (Chenopodiaceae): diversification, biogeography, and evolutionary trends in leaf and flower morphology

Abstract

Chenopodiaceae‐Salicornioideae (14–16 gen./c. 90 spp.) are distributed worldwide in coastal and inland saline habitats. Most of them are easy to recognize by their succulent‐articulated stem with strongly reduced leaves and by flowers aggregated in dense, thick spike‐shaped thyrses. ITS and the atpB‐rbcL spacer were sequenced for 67 species representing 14 genera of Salicornioideae and analysed with maximum parsimony and maximum likelihood, a fossil‐calibrated molecular clock using the penalized likelihood method, and lineage through time plots. The evolution of stem, leaf, and flower morphology was traced using MacClade. Both molecular markers indicate that the monophyletic Salicornioideae originated in Eurasia during the Late Eocene/Early Oligocene (38.2–28.7 Mya) and experienced a rapid radiation into its major lineages during the Early Oligocene with Allenrolfea/Heterostachys, Kalidium, Halopeplis and Halocnemum/Halostachys branching off early. Already in the Middle Miocene (19.6–14.6 Mya) all major lineages of Salicornioideae were present. These additionally include Arthrocnemum/Microcnemum, the Halosarcia lineage (which includes all Australian species except for the Australian Sarcocornia) and the Salicornia/Sarcocornia lineage. A high intercontinental dispersability can be observed in Salicornioideae in particular in the Salicornia/Sarcocornia lineage with multiple colonization events in America, Australia and South Africa linked to the global aridification during the Oligocene, Late Miocene and Pliocene. The comparatively low species number of many genera is explained by a low number of niches present in the extreme habitats of Salicornioideae, strong interspecific competition mainly by close relatives, and by Pleistocene extinctions. We detected an evolutionary trend towards increasing reduction of the leaf lamina in Salicornioideae, with an ovate or terete leaf with a decurrent base as the plesiomorphic condition. Opposite phyllotaxis has arisen at least two times in the subfamily and is strongly correlated with the pair‐wise fusion of leaves (not bracts), the reduction of leaf lamina, and the articulation of stem. However, the articulated stems and reduced leaves also have evolved twice in lineages with alternate phyllotaxis, such as Allenrolfea and Kalidium caspicum. Only one shift from free to connate bracts occurred in Salicornioideae with at least one reversal within the Halosarcia lineage. The fusion of bracts is mostly accompanied by a partly or fully connation of bracts and axis resulting in club‐shaped spikes in which the flwers are tightly embedded in cavities. Both molecular trees are conflicting with the traditional tribes indicating that their diagnostic characters have originated by convergent evolution. For reasons of stability and clarity we propose that only one tribe, Salicornieae, should be recognized. The traditional circumscription of most genera is supported by the molecular results except for the closely related genera of the Australian Halosarcia clade and the Sarcocorni...

Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture

“…Kadereit and co-workers have analyzed diversification, biogeography and evolutionary trends in leaf and flower morphology of Salicornioideae and Chenopodioideae. About 90 species have been described occurring worldwide in coastal and saline habitats (Kadereit et al, 2006). Using maximum parsimony and maximum likelihood, a fossil-calibrated molecular clock and lineage through time plots, it was demonstrated that the monophyletic Salicornioideae originated in Eurasia along the northern margin of the Tethys Sea during the Late Eocene and Early Oligocene (38.2-28.7 Mya, Table 2, Kadereit et al, 2006) and experienced a rapid radiation into its major lineages during the Early Oligocene.…”

“…About 90 species have been described occurring worldwide in coastal and saline habitats (Kadereit et al, 2006). Using maximum parsimony and maximum likelihood, a fossil-calibrated molecular clock and lineage through time plots, it was demonstrated that the monophyletic Salicornioideae originated in Eurasia along the northern margin of the Tethys Sea during the Late Eocene and Early Oligocene (38.2-28.7 Mya, Table 2, Kadereit et al, 2006) and experienced a rapid radiation into its major lineages during the Early Oligocene. This was after the end of warm humid period of the Middle Palaeocene to Early Eocene and the start of a long period of decreasing temperatures and increasing aridity (Willis and McElwain, 2002).…”

“…Mya = million years ago, time estimates based on molecular clock analysis calibrated with macro fossil findings. Based on Kadereit et al (2003Kadereit et al ( , 2006Kadereit et al ( , 2007 set, seed polymorphism, high germination rates and good seedling establishment (Ungar, 1982(Ungar, , 1987.…”

Taxonomical identity of <em>Sarcocornia fruticosa</em> and <em>S. hispanica</em> in the Iberian Peninsula

“…Scott (Amaranthaceae) is a markedly complex genus as has been reported by many authors (Castroviejo & Coello, 1980;Castroviejo & Lago, 1992;Shepherd & Yan, 2003;Kadereit & al., 2006;Alonso & Crespo, 2008), and a large number of synonyms is recognized due to its taxonomical difficulty (Maire & Quézel, 1962;Quézel & Santa, 1963;Meikle, 1977;Pignatti, 1982;Bolòs & Vigo, 1990;Ball, 1993;Coste, 2007;Guilló & al., 2011). The marked halophytic behaviour of Sarcocornia species favours the development of similar morphological traits, which makes quite difficult to distinguish species, and even other related genera (e.g.…”

An up-to-date familial and suprafamilial classification of succulent plants

“…At least xerohalophytic taxa have a well-founded claim to succulence. Stem succulence is either cortical (with an outer palisade-like layer, and a central water-storage parenchyma; Fahn & Cutler, 1992), or derived from sheathing leaf bases ("false" stem succulence) (Kadereit et al, 2006). Weakly expressed leaf succulence is common, and in terete leaves (e.g.…”