When do different C₄ leaf anatomies indicate independent C₄ origins? Parallel evolution of C₄ leaf types in Camphorosmeae (Chenopodiaceae)
2014
Kadereit, Gudrun | Lauterbach, Maximilian | Pirie, Michael D. | Arafeh, Rami | Freitag, Helmut
Broad-scale phylogenetic studies give first insights in numbers, relationships, and ages of C₄ lineages. They are, however, generally limited to a model that treats the evolution of the complex C₄ syndrome in different lineages as a directly comparable process. Here, we use a resolved and well-sampled phylogenetic tree of Camphorosmeae, based on three chloroplast and one nuclear marker and on leaf anatomical traits to infer a more detailed picture of C₄ leaf-type evolution in this lineage. Our ancestral character state reconstructions allowed two scenarios: (i) Sedobassia is a derived C₃/C₄ intermediate, implying two independent gains of C₄ in Bassia and Camphorosma; or (ii) Sedobassia is a plesiomorphic C₃/C₄ intermediate, representing a syndrome ancestral to the Bassia/Camphorosma/Sedobassia lineage. In Bassia, a kochioid leaf type (Bassia muricata and/or Bassia prostrata type) is ancestral. At least three independent losses of water-storage tissue occurred, resulting in parallel shifts towards an atriplicoid leaf type. These changes in leaf anatomy are adaptations to different survival strategies in steppic or semi-desert habitats with seasonal rainfall. In contrast, Camphorosma shows a fixed C₄ anatomy differing from Bassia types in its continuous Kranz layer, which indeed points to an independent origin of the full C₄ syndrome in Camphorosma, either from an independent C₃ or from a common C₃/C₄ intermediate ancestor, perhaps similar to its C₃/C₄ intermediate sister genus Sedobassia. The enlarged bundle sheath cells of Sedobassia might represent an important early step in C₄ evolution in Camphorosmeae.
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