Vascular variants in seed plants-a developmental perspective

Abstract

Over centuries of plant morphological research, biologists have enthusiastically explored how distinct vascular arrangements have diversified. These investigations have focused on the evolution of steles and secondary growth and examined the diversity of vascular tissues (xylem and phloem), including atypical developmental pathways generated through modifications to the typical development of ancestral ontogenies. A shared vernacular has evolved for communicating on the diversity of alternative ontogenies in seed plants. Botanists have traditionally used the term 'anomalous secondary growth' which was later renamed to 'cambial variants' by late Dr. Sherwin Carlquist (1988). However, the term 'cambial variants' can be vague in meaning since it is applied for developmental pathways that do not necessarily originate from cambial activity. Here, we review the 'cambial variants' concept and propose the term 'vascular variants' as a more inclusive overarching framework to interpret alternative vascular ontogenies in plants. In this framework, vascular variants are defined by their developmental origin (instead of anatomical patterns), allowing the classification of alternative vascular ontogenies into three categories: (i) procambial variants, (ii) cambial variants and (iii) ectopic cambia. Each category includes several anatomical patterns. Vascular variants, which represent broader developmental based groups, can be applied to both extant and fossil plants, and thereby offer a more adequate term from an evolutionary perspective. An overview of the developmental diversity and phylogenetic distribution of vascular variants across selected seed plants is provided. Finally, this viewpoint discusses the evolutionary implications of vascular variants.

Keywords: cambium; development; ectopic cambia; evolution; meristems; plant anatomy; procambium; vascular tissue.

Figure 1.

Stem vascular arrangements in angiosperms illustrating the typical growth and vascular variants. (A) Typical eustele; Portulaca halimoides, Portulacaceae; courtesy of Thaíla V. A. Santos. (B) Regular secondary growth; Paullinia coriacea, Sapindaceae; courtesy of Robson G. Silva. (C) Eustele with medullary bundles (in the centre of the pith) and continuous procambium forming additional vascular bundles in the periphery; Allionia incarnata, Nyctaginaceae. (D) Atactostele; Commelina platyphylla, Commelinaceae; courtesy of Ricardo S. B. Vita. (E) Non-cylindrical stem resulting from atypical cambial activity (single cambium); Schnella sp. Fabaceae; courtesy of Caian S. Gerolamo. (F) Phloem wedges resulting from atypical cambial activity (single cambium); Mansoa difficilis, Bignoniaceae; courtesy of Caian S. Gerolamo. (G) Compound stem originating from atypical procambial patterning, generating a central cylinder and nine peripheral vascular cylinders, each with its own cambium (multiple cambia); Serjania fuscifolia, Sapindaceae; courtesy of Robson G. Silva. Images not to scale.

Figure 2.

Medullary bundles (procambial variant) and interxylary phloem (cambial variant) in stems of Nyctaginaceae. (A, B). Primary growth with medullary bundles and developing vascular bundles (arrows) derived from the continuous procambium (ring of smaller cells). Commicarpus scandens. (C) Early secondary growth showing medullary bundles and cambium developed from the vascular bundles derived from the continuous procambium. Acleisanthes chenopodioides. (D) Note that the phloem of vascular bundles derived from the continuous procambium become the first ‘phloem islands’ and, therefore, there is no formation of a continuous vascular cylinder of secondary xylem and secondary phloem. Guapira pernambucensis. (E) Medullary bundles and atypical cambial activity producing ‘phloem islands’ within the wood. (F) Adult stem showing medullary bundles with secondary growth, absence of continuous vascular cylinder, and multiple ‘phloem islands’. Pisoniella glabrata. (A–F) Light microscopy. (A–D, F) Stained with Safranin and Astra Blue. (E) Stained with Toluidine Blue.

Figure 3.

External vascular cylinders in stems of Piperaceae, a case of procambial variant. This ontogeny originates from medullary bundles which undergo secondary growth. (A) Stem during primary growth showing three rings of medullary bundles (three successive coloured rings/green). (B) Mature stem showing medullary bundles in the pith (coloured ring in the center/green), continuous secondary growth derived from a cambium originated from the middle ring of medullary bundles, and isolated ‘external vascular cylinders’ (coloured ring in the periphery/brown) derived from the outer ring of medullary bundles. Small circles indicate vessels in the xylem and dotted area indicates the phloem. Figures not to scale.

Figure 4.

Compound stems in Sapindaceae, a case of procambial variant. (A) Illustration based on stems of many Serjania species during transition from primary to secondary growth; each lobe has multiple vascular bundles from which a vascular cambium develops generating a peripheral vascular cylinder (coloured circles in the periphery/pink); a central vascular cylinder is also produced from vascular bundles in the usual position (coloured circle in the center/blue; see also Fig. 1G). (B) Illustration based on stems of many Paullinia species during transition from primary to secondary growth; a central vascular cylinder is formed in the usual way (coloured circle in the center/blue), and peripheral vascular cylinders derive from a cambium initiating from a single isolated vascular bundle (coloured circles in the periphery/pink); in this case, three isolated bundles will generate three peripheral vascular cylinders. (C) Mature stem with a central vascular cylinder and three peripheral vascular cylinders. Paullinia spicata. Small circles indicate vessels in the xylem and dotted area indicates the phloem. Figures not to scale.

Figure 5.

Divided stem in Sapindaceae initiate with atypical procambial patterning. (A) Drawing illustrating young stem with lobed conformation and vascular bundles distributed along the lobes. Figures not to scale. (B) Light microscopy of Serjania deflexa showing two cambia generating two peripheral vascular cylinders; each cambium and peripheral vascular cylinder is derived from vascular bundles in one lobe. Stained with Toluidine Blue. Courtesy of Neusa Tamaio. (D) Macroscopic image of adult stem of Serjania corrugata showing five peripheral vascular cylinders and no central cylinder. Stem diameter: 15 mm. Courtesy of Robson G. Silva. Small circles indicate vessels in the xylem and dotted area indicates the phloem. sph, secondary phloem; sxy, secondary xylem.

Figure 6.

Synthesis of vascular variants categories and their respective anatomical patterns based on the known diversity across seed plants. Only some anatomical patterns are represented in the right side for each category—a complete list of anatomical patterns associated to each category can be found in Supporting Information—Table S1. Drawings of anatomical patterns are inspired from cross sections of species of the following families: medullary bundles: Nyctaginaceae, compound stem: Sapindaceae, atactostele: Commelinaceae, interxylary phloem: Nyctaginaceae, phloem wedges: Bignoniaceae, lobed stem: Sapindaceae, neoformations: Rubiaceae, successive cambia: Fabaceae, corded stem: Sapindaceae. Small circles indicate vessels in the xylem and dotted area indicates the phloem.

Figure 7.

Neoformations in stems of Dalechampia (Euphorbiaceae), a case of ectopic cambia. (A, B) Dalechampia alata. (A) Adult stem showing the initiation of an ectopic cambia (arrow) from vascular parenchyma at the periphery of the non-conducting phloem. (B) Detail of ectopic cambia (arrow) initiation. (C) Line drawing of mature stem showing multiple ectopic cambia generating neoformations (yellow) at the periphery of the vascular cylinder. Small circles indicate vessels in the xylem and dotted area indicates the phloem. sph, secondary phloem; sxy, secondary xylem. (B, C) Stained with Safranin and Astra Blue.

Figure 8.

Distribution of vascular variants in the phylogeny of seed plants. Tree topology follows Stevens (2001 onwards) for angiosperms and Li et al. (2021) for gymnosperms. All types of ‘cambial variants’ presented by Angyalossy et al. (2015) are distributed in one of the three categories of vascular variants [see  Supporting Information—Table S2 for additional details]. The ‘monocot cambium’ is indicated for their respective orders and the atactostele is indicated in the branch leading to the monocot lineage.