title: When do different C4 leaf anatomies indicate independent C4 origins? Parallel evolution of C4 leaf types in Camphorosmeae (Chenopodiaceae).
abstract: 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.
authors.affiliation: Institut für Allgemeine und Spezielle Botanik und Botanischer Garten der Johannes Gutenberg-Universität Mainz, D-55099 Mainz, Germany clausing@uni-mainz.de.
authors.forename: Gudrun
authors.initials: G
authors.lastname: Kadereit
authors.affiliation: Institut für Allgemeine und Spezielle Botanik und Botanischer Garten der Johannes Gutenberg-Universität Mainz, D-55099 Mainz, Germany.
authors.forename: Maximilian
authors.initials: M
authors.lastname: Lauterbach
authors.affiliation: Institut für Allgemeine und Spezielle Botanik und Botanischer Garten der Johannes Gutenberg-Universität Mainz, D-55099 Mainz, Germany Department of Biochemistry, University of Stellenbosch, Matieland 7600, South Africa.
authors.forename: Michael D
authors.initials: MD
authors.lastname: Pirie
authors.affiliation: Biotechnology Research Center, Palestine Polytechnic University, PO Box 198, Hebron, Palestine.
authors.forename: Rami
authors.initials: R
authors.lastname: Arafeh
authors.affiliation: Institut für Biologie, Arbeitsgruppe Systematik und Morphologie der Pflanzen, Universität Kassel, D-34109 Kassel, Germany.
authors.forename: Helmut
authors.initials: H
authors.lastname: Freitag
mesh_terms: D005075:Biological Evolution; D002244:Carbon / Q000378:metabolism; D019663:Chenopodiaceae / Q000033:anatomy & histology / Q000235:genetics* / Q000502:physiology; D008961:Models, Structural; D010788:Photosynthesis; D010802:Phylogeny; D018515:Plant Leaves / Q000033:anatomy & histology / Q000235:genetics / Q000502:physiology; D058526:Plant Vascular Bundle / Q000033:anatomy & histology / Q000235:genetics / Q000502:physiology; D014867:Water / Q000502:physiology*
chemical_list: D014867:Water; D002244:Carbon
keywords: Bassia; C4 photosynthesis; Camphorosma; Kranz anatomy; Sedobassia; bundle sheath; water-storage tissue.