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: (1) procambial variants, (2) cambial variants and (3) 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, the evolutionary implications of vascular variants are discussed.

Gelatinous fibers develop asymmetrically for posture support of bends and coils in common bean vine

“…Many vines have highly modified stem anatomies, including wholesale reorganization of the vascular tissues (Angyalossy, Pace and Lima, 2014; Cunha Neto, 2023), but common bean stems have a typical eustele and regular secondary growth. Therefore, the only clear anatomical candidate related to climbing in this species are the G-fibers; their presence has been previously reported (Chery et al 2021; Chernova et al, 2023).…”

“…Many vines have highly modified stem anatomies, including wholesale reorganization of the vascular tissues (Angyalossy, Pace and Lima, 2014;Cunha Neto, 2023), but common bean stems have a typical eustele and regular secondary growth.…”

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

“…While this typical development results in stems with homogeneous amounts of wood (secondary xylem) and inner bark (secondary phloem) in most extant seed plants, many lineages have evolved alternative developmental pathways (=ontogeny) that deviate from this typical vascular architecture. These alternative ontogenies lead to anatomical modifications in the rate and/or organization of vascular tissues due to changes in the location, organization, and activity of vascular meristems in the plant axis and are here referred to as vascular variants (previously known as “anomalous growth” or “cambial variants”; Cunha Neto, 2023). Besides generating considerable morphological diversity, the study of vascular variants has gained notoriety due to their adaptive roles in climbing plants (e.g., flexibility, conductivity, injury repair, and mechanical resistance; Carlquist, 1991, 2013; Fisher and Ewers, 1991; Rowe et al, 2004) and self-supporting plants including evidence from mangrove trees (e.g., adaptation to dynamic mangrove environment; Robert et al, 2014) or herbaceous species (e.g., alternative routes for increased hydraulic conductivity through medullary bundles; Cunha Neto et al, 2023).…”

Medullary bundles in Caryophyllales: form, function, and evolution

“…beets and quinoa) and is distinguished by the repeated evolution of unusual ecological adaptations, including succulents, gypsophilous and carnivorous plants (Hernández‐Ledesma et al ., 2015; Walker et al ., 2018). Some Caryophyllales also contain betalain pigments instead of anthocyanin (Brockington et al ., 2015; Timoneda et al ., 2019), have unique flower development (Brockington et al ., 2009; Ronse de Craene, 2021), diverse fruit types (Sukhorukov et al ., 2015), and vascular variants (Cunha Neto, 2023), markedly the anatomical pattern called successive cambia (Carlquist, 2010; Timonin, 2011). Also considered as a procambial variant (Cunha Neto, 2023), medullary bundles are another striking anatomical feature in the vascular system of Caryophyllales.…”

“…Some Caryophyllales also contain betalain pigments instead of anthocyanin (Brockington et al ., 2015; Timoneda et al ., 2019), have unique flower development (Brockington et al ., 2009; Ronse de Craene, 2021), diverse fruit types (Sukhorukov et al ., 2015), and vascular variants (Cunha Neto, 2023), markedly the anatomical pattern called successive cambia (Carlquist, 2010; Timonin, 2011). Also considered as a procambial variant (Cunha Neto, 2023), medullary bundles are another striking anatomical feature in the vascular system of Caryophyllales. They occur in many charismatic plants of Cactaceae (cacti), Droseraceae (sundews), Nepenthaceae (pitcher plants), and Nyctaginaceae (4 o'clock; DeBuhr, 1977; Mauseth, 1993; Schwallier et al ., 2017; Cunha Neto et al ., 2020a).…”