MOLECULAR PHYLOGENY OF ATRIPLICEAE (CHENOPODIOIDEAE, CHENOPODIACEAE): IMPLICATIONS FOR SYSTEMATICS, BIOGEOGRAPHY, FLOWER AND FRUIT EVOLUTION, AND THE ORIGIN OF C4 PHOTOSYNTHESIS

Premise of the study : Atripliceae (Chenopodiaceae), including Atriplex (300 spp.) as the largest genus of the family, are an ecologically important group of steppes and semideserts worldwide. Relationships in Atripliceae are poorly understood due to obscure and potentially convergent morphological characters. Methods : Using sequence variation of two chloroplast markers (rbcL gene, atpB-rbcL spacer) and one nrDNA marker (ITS) analyzed with BEAST, we investigated the systematics and biogeography of Atripliceae. We surveyed flower morphology and fruit anatomy to study the evolution of flowers and fruits in the tribe. Key results : Female flowers with persistent foliar cover (the diagnostic character of traditional Atripliceae) evolved three times in Chenopodioideae, in Atripliceae s.s., Axyrideae, and Spinacia. Atripliceae s.s. started to diversify during the Early Miocene in Eurasia, separating into the Archiatriplex and the Atriplex clades. The former consists of eight species-poor, disjunct, and morphologically heterogeneous genera and is likely a relictual lineage. The Atriplex clade comprises the majority of species and evolved one C-4 lineage 14.1-10.5 Ma, which diversified rapidly worldwide. The C-4 Atriplex entered North America during the Middle/Late Miocene and spread to South America subsequently. Australia was colonized by two C-4 lineages both arriving during the Late Miocene. One of them diversified rapidly, giving rise to most Australian Atriplex species. Conclusions : Atripliceae s.s. comprise Archiatriplex, Atriplex, Exomis, Extriplex, Grayia, Halimione, Holmbergia, Manochlamys, Proatriplex, and Stutzia. Microgynoecium is included based on morphology but only weak molecular support. Axyris, Krascheninnikovia, and Ceratocarpus (here described as Axyrideae) and Spinacia are excluded from Atripliceae.