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Is Pteropyrum a pathway to C4 evolution in Polygonaceae? An integrative approach to the taxonomy and anatomy of Pteropyrum (C3), an immediate relative of Calligonum (C4)

Abstract : Pteropyrum is a small genus of Polygonaceae with four species from the arid regions of Iran and adjacent countries. Pteropyrum spp. are not precisely delimitated and are difficult to identify because of their high plasticity in morphological characters. Pteropyrum (C 3) has a close affinity to Calligonum (C 4) and is therefore a suitable case for C 4 evolutionary studies. We investigated the morphology and micromorphology (including pollen morphology) of Pteropyrum and elucidated the phylogenetic relationships with Atraphaxis and Calligonum using nuclear ITS sequences. Characteristics of the photosynthetic tissues such as volume and number of layers of primary carbon assimilation tissues (PCA) and photosynthetic carbon reduction tissue (PCR) were studied. In addition, the leaf and cotyledon anatomical characters of Pteropyrum (C 3), Atraphaxis (C 3) and Calligonum (C 4), and their δ 13 C values were compared to look for evolutionary changes in assimilating organs. The molecular phylogenetic tree identifies two strongly supported clades in Pteropyrum and its close relationship with Calligonum, confirming previous studies. Some morphologically similar species belong to different clades, which is probably due to convergent evolution and homoplasy. Leaf anatomical studies show that Atraphaxis has a multilayered mesophyll tissue, whereas Calligonum has one-layered mesophyll cells. The volume and layer number of mesophyll tissue cells decreases, whereas water storage tissue area significantly increases from Atraphaxis to Pteropyrum and Calligonum. This phenomenon confirms previous studies in other lineages with C 4 salsoloid anatomy that have evolved through increasing of water storage tissue and succulence of assimilating organs. In the taxonomic part of the paper, a key to identification of accepted taxa of Pteropyrum, description of species and distribution maps are presented based on numerous herbarium specimens and our own rich collections from the field. Four new species are described based on a combination of morphology of seedlings and mature plants, pollen morphology and molecular data. A subspecific classification is suggested to show morpho-geographical variation of Pteropyrum aucheri s.l.
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Moslem Doostmohammadi, Maryam Malekmohammadi, Morteza Djamali, Hossein Akhani. Is Pteropyrum a pathway to C4 evolution in Polygonaceae? An integrative approach to the taxonomy and anatomy of Pteropyrum (C3), an immediate relative of Calligonum (C4). Botanical Journal of the Linnean Society, Linnean Society of London, 2019, 20, pp.1-32. ⟨10.1093/botlinnean/boz079⟩. ⟨hal-02391348⟩

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