Phylogenetic relationships in the Salicornioideae/Suaedoideae/Salsoloideae s.l. (Chenopodiaceae) Clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets

The Chenopodiaceae includes taxa with both C-3 and C-4 photosynthesis with diverse kinds of Kranz anatomy and single-celled C-4 species without Kranz anatomy; thus, it is of key importance for understanding evolution of C-4 photosynthesis. All of the C-4 genera except Atriplex, which belongs to Chenopodioideae, are in the Salicornioideae/Suaedoideae/Salsoloideae s.l. (including Camphorosmeae and Sclerolaeneae) clade. Our study focused on the relationships of the main lineages within this clade with an emphasis on the placement of the single cell functioning C-4 genus Bienertia using maximum parsimony, maximum likelihood, and Bayesian inference phylogenetic analyses of the nuclear ribosomal ITS and five chloroplast DNA regions (atpB-rbcL, matK, psbB-psbH, rbcL, and trnL-trnF). Further we provide a detailed phylogeny of Alexandra and Suaeda based on ITS, atpB-rbcL, and psbB-psbH. Our molecular data provide strong statistical support for the monophyly of: (1) a Salicornioideae/Suaedoideae/Salsoloideae s.l. clade; (2) a Salicornioideae/Suaedoideae clade; (3) the subfamilies Salicornioideae, Suaedoideae (including Bienertia) and Salsoloideae s.l.; (4) the tribes Suaedeae, Salsoleae, and Camphorosmeae; (5) the Salicornieae if Halopeplideae is included; and (6) Suaeda if Alexandra is included. Alexandra lehmannii is therefore reclassified as Suaeda lehmannii and a new section of Suaeda is created, section Alexandra. There are four independent origins of C-4 photosynthesis within the Suaedoideae including two parallel origins of Kranz C-4 anatomy (in Suaeda sections Salsina s.l. and Schoberia) and two independent origins of C-4 systems without Kranz anatomy (in Bienertia and in Suaeda section Borszczowia).