Repeated evolution of endoscopic peripheral vascular bundles in succulent leaves of Aizoaceae (Caryophyllales)

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Abstract
We investigated the presence and orientation of peripheral vascular bundles in leaves of 81 species representing 72 genera of Aizoaceae. Our study included a wide range of morphological shapes of leaves sampled from all four subfamilies of Aizoaceae, with an emphasis on succulent leaves found in Mesembryanthemoideae and Ruschioideae. Our anatomical studies revealed that only three of the four subfamilies in Aizoaceae have peripheral vascular bundles in their leaves, i.e., Sesuvioideae, Mesembryanthemoideae and Ruschioideae. Apart from Sesuvium (Sesuvioideae), all other species with peripheral vascular bundles have an endoscopic orientation, i.e., the phloem is positioned closer to the epidermis, whereas the xylem is pointing towards the interior of the leaf. This contrasts the situation in other Caryophyllales, where, with the exception of Borszczowia (Amaranthaceae), two different types of three‐dimensional venations were observed. The distinct types of three‐dimensional venation may in turn provide clues to the different pathways by which the similar leaves evolved. Endoscopic peripheral vascular bundles in Aizoaceae were only found in species with an expanded leaf base and (sub‐)cylindrical to trigonous leaves. Although flat‐bladed species of Aizoaceae generally have no peripheral vascular bundles, they were present in Delosperma tradescantioides (Ruschioideae: Ruschieae). Persistent, flat leaves are very rare within the hyperdiverse Ruschieae, which typically have (sub‐)cylindrical to trigonous leaves. Thus, the presence of peripheral vascular bundles in leaves of D. tradescantioides indicates that flat‐bladed, persistent leaves constitute a reversal within tribe Ruschieae. The additional presence of lateral bundles in the outer lamina of leaves of D. tradescantioides can be interpreted as a regain of planate venation. Mapping the evolution of peripheral vascular bundles onto a phylogeny of the Aizoaceae suggests that this character evolved repeatedly within subfamilies Mesembryanthemoideae and Ruschioideae.

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