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

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.

Phylogeny of Sesuvioideae (Aizoaceae) – Biogeography, leaf anatomy and the evolution of C4 photosynthesis

“…Succulence is common to all of the subfamilies of the Aizoaceae. Ruschioideae, Mesembryanthemoideae and Aizooideae differ from Sesuvioideae by an endoscopic orientation of the peripheral vascular bundles (Melo-de-Pinna et al, 2014).…”

Vegetative morphology and anatomy ofMaundia(Maundiaceae: Alismatales) and patterns of peripheral bundle orientation in angiosperm leaves with three-dimensional venation

“…A; = 3D type II of Ogburn & Edwards, ): all peripheral bundles with xylem facing the adaxial leaf side and phloem facing the abaxial side, so that none of them are inverted. I/N/N‐Type (Fig. B; = endoscopic arrangement of peripheral bundles of Melo‐de‐Pinna et al ., ): all peripheral bundles with phloem facing the nearest leaf surface, so that the peripheral bundles on the adaxial side are inverted and bundles on the abaxial side are normally oriented. N/N/I‐Type (Fig. C; = 3D type II of Ogburn & Edwards, ; = exoscopic arrangement of peripheral bundles of Melo‐de‐Pinna et al ., ): all peripheral bundles with xylem facing the nearest leaf surface, so that the peripheral bundles on the abaxial side are inverted. I/N/I‐Type (Fig.…”

“…As in core Alismatales, in the distantly related core eudicot Caryophyllales, small peripheral bundles of thick leaves do not represent the entire conductive system, but supplement a system of central, normally oriented larger bundles or a single central bundle (Butnik et al ., ; Freitag & Stichler, ; Ogburn & Edwards, ; Freitag & Kadereit, ; Melo‐de‐Pinna et al ., ; Hernandes‐Lopes, Oliveira‐Neto & Melo‐de‐Pinna, ). Patterns of variation in orientation of peripheral bundles are identical in those Alismatales and Caryophyllales that possess small bundles along the entire leaf surface.…”

“…ex F.A.C.Weber) K.Schum. ], Kewaceae and Halophytaceae (Butnik et al ., ; Kadereit et al ., ; Voznesenskaya et al ., ; Ogburn & Edwards, ; Freitag & Kadereit, ; Melo‐de‐Pinna et al ., ; Hernandes‐Lopes et al ., ).…”

“…This arrangement of bundles in leaves directly continues the orientation of leaf traces in the stem. Inverted collateral vascular bundles are known in leaves of various plants, especially in monocots and the eudicot order Caryophyllales, in which several patterns of arrangement and formation of inverted bundles are found (Arber, ; Cutler, ; Fisher, ; Tomlinson, ; Ogburn & Edwards, ; Mashayekhi & Columbus, ; Melo‐de‐Pinna et al ., ).…”