Ontogeny of divided vascular cylinders in Serjania: the rise of a novel vascular architecture in Sapindaceae

Abstract

Sapindaceae lianas are remarkable for the diversity of cambial variants found in their stems. One of the family’s exclusive cambial variant is the divided vascular cylinder, which occurs in eight species of the genus Serjania. This cambial variant is marked by 5 peripheral vascular cylinders around a large pith. We performed a comparative developmental analysis, integrating traditional plant anatomy techniques with high-resolution X-ray micro-computed tomography to investigate the structure and development of the stems of three species with divided vascular cylinder. Our observations showed that the initial stages of stem development were similar to those described in the literature, however, on later developmental stages a central vascular cylinder appears in all species. The ontogeny of these stems are marked by three main processes: (i) dissection of vascular tissue from the peripheral vascular cylinders; (ii) development of new cambial arcs through the redifferentiation of pith cells; and (iii) recruitment of cambial cells from the inner portions of the vascular cambium of the peripheral vascular cylinders, forming a novel central vascular cylinder where the pith was, surrounded by five initial peripheral cylinders. As an ulterior developmental stage, some older stems also develop neoformations and connections between the different vascular cylinders. While our findings support previous descriptions of divided vascular cylinders, this is the first study illustrating the formation of the central vascular cylinder in this cambial variant. Our observations further corroborate that Serjania is the lineage with the highest and some of the most complex forms of cambial variants among all vascular plants.

The “abominable mystery” of Schenck: the polymorphism ofSerjania piscatoriaand its implications for the evolution of vascular variants in Paullinieae (Sapindaceae)

“…In the stem of S. piscatoria, these new cambia frequently generate circular units irregularly distributed along the circumference of the stem (in addition to eventual peripheral cylinders derived from the isolated vascular bundle). This pattern is a typical case of neoformationsnew cambia forming independent, circular vascular units in an irregular fashion (Cunha Neto and Onyenedum, 2023)similar to that described for stems (Tamaio and Angyalossy, 2009;Cunha Neto et al, 2018;Rizzieri et al, 2021) and roots (Bastos et al, 2016) of other Paullinieae species, and other families (e.g., Rubiaceae, Leal et al, 2020). In both S.…”

“…pernambucensis Radlk., and some Paullinia species; Cunha Neto et al, 2018) or in combination with other variants, as observed with the emergence of neoformations in species with divided (Rizzieri et al, 2021) and compound stem (Tamaio and Angyalossy, 2009). Previous studies on the evolution of development have shown that ectopic cambia evolved only once in Paullinia (= successive cambia; Chery et al, 2020) and once in Urvillea (Cunha .…”

“…piscatoria and other Paullinieae species, neoformations are produced after the establishment of other patterns of vascular variants, including successive cambia (Cunha Neto et al, 2018), which is also a type of ectopic cambia, as well as divided stems (Rizzieri et al, 2021), and compound stems (Tamaio and Angyalossy, 2009), which are cases of procambial variants (Cunha Neto 2023). Regarding their origin, neoformations arise from vascular parenchyma in Paullinieae, but in lianas from other families they may originate from the cortex (e.g., Rubiaceae, Leal et al, 2020).…”

Laser ablation tomography (LATscan) as a new tool for anatomical studies of woody plants

“…To gain a structural understanding of vascular systems, 3D reconstructions were introduced with the development of the shuttle technique (Zimmermann & Tomlinson, 1966), and recently 3D visualization has been made using especially X‐ray microtomography (Bastos et al ., 2016; Cunha Neto et al ., 2018, 2020; Rizzieri et al ., 2021; Mylo et al ., 2021a). Specifically, X‐ray microtomography has been largely improved and successfully used to generate 2D and 3D information of xylem networks, which is possible also through in vivo , nondestructive analyses (Brodersen, 2013; Wason et al ., 2017, 2021; Brodersen et al ., 2018).…”

Laser ablation tomography (LATscan) as a new tool for anatomical studies of woody plants

“…Moreover, wood and bark are complex tissues composed of cells with unique contents (e.g., phenolics, starch), and cell wall composition (e.g., cellulose, lignin, suberin), therefore multiple stains must be used to extract these data. Other complex traits that are challenging to understand through traditional anatomical methods are vascular variants i.e., alternative patterns of vascular growth generating odd and intricate morphologies (Bastos et al ., 2016; Cunha Neto et al ., 2018; Rizzieri et al ., 2021), or plant-parasitic interactions where the parasite obtain water and nutrients from the host plant through the complex and dynamic structure, the haustorium (Teixeira-Costa & Ceccantini, 2016; Mylo et al ., 2021), respectively. To gain a structural understanding of these complex networks, 3D reconstructions have been made using X-ray microtomography (Fig.…”