Comparative systematic study of colleters and stipules of Rhizophoraceae with implications for adaptation to challenging environments

Abstract

Colleters are multicellular secretory structures found on various organs in flowering plants. Colleters on the adaxial sides of stipules have been hypothesized to play a role in protecting the developing shoot. Rhizophoraceae is a stipulate family with a broad distribution from mangrove to montane environments, which makes the family well suited for the examination of this hypothesis, but the colleters of Rhizophoraceae are not well known. We compared species from all three tribes of Rhizophoraceae, including five inland genera and all four mangrove genera. In all species, several to hundreds of colleters, sessile or stalked, arranged in rows aggregated in genus-specific shapes, are found at the adaxial bases of open and closed stipules. Pellacalyx uniquely has additional colleters at the stipule margins. Colleters are all of the standard type, comprising a central axis of core parenchyma with large vacuoles and tannins, and an outer palisade-like epidermis with organelles involved in secretory activity. An exception is Pellacalyx axillaris, in which colleters appear as extremely small epidermal protrusions. Kandelia obovata has a tracheary element in some colleters. Pellacalyx uniquely has an unusual fleshy outgrowth on the adaxial stipule base. We propose an evolutionary sequence in which Macarisia has plesiomorphic stipule and colleter traits and the mangrove Kandelia obovata with colleter vascular traces is most derived. Colleter and stipule structures are largely concordant with habitat and phylogeny, and show taxonomic value. The strong alignment of colleter and stipule patterns with habitat is suggestive that colleters have a protective function, although some components of these patterns may be phylogenetically determined.

Foliar secretory structures in Crotoneae (Euphorbiaceae): Diversity, anatomy, and evolutionary significance

“…The occurrence of druses in the parenchyma of the colleter central axis in all studied species is a character with potential taxonomic value within Euphorbiaceae or even in Malpighiales. In fact, within the other families in this order, druses have been reported in the core parenchyma region of colleters in Rhizophoraceae (Sheue et al, 2012, 2013), whereas they are absent in the colleters of Caryocar brasiliense Cambess. in the Caryocaraceae (Paiva and Machado, 2006).…”

Colleters in Rubiaceae from forest and savanna: the link between secretion and environment

“…Although some colleter characteristics (e.g. morphology, number and distribution) may be phylogenetically determined (Sheue et al 2012(Sheue et al , 2013, some studies have reported changes in colleters' functional performance traits associated with environment, which suggests that there is an ecological constraint related to the role of secretion in natural conditions (Sheue et al 2012(Sheue et al , 2013Tresmondi et al 2015). By comparing members of Rubiaceae growing in contrasting vegetation types (forest and savanna), we found that colleters similar in morphology and anatomical organisation differ in the chemical composition of secretions (Tresmondi et al 2015).…”

Bruguiera × rhynchopetala (Rhizophoraceae) newly reported in India, far west of south-east Asian, east Asian and western Pacific regions

“…We are aware of other potentially diagnostic characters, like the colleters at the base of the conspicuous interpetiolar stipules of this genus (Hou, 1958;Sheue et al, 2013). However, for this assessment, we have relied on morphological characters known to be diagnostic for comparable taxa within this genus worldwide (Duke & Ge, 2011;Cooper et al, 2016;Duke & Kudo, 2018) Reports until now revealed the existence of a hybrid intermediate only in countries in the eastern portion of the parental overlap zone in both northern and southern hemispheres like southern China, Malesia, Papua New Guinea and northern Australia (Duke & Ge, 2011;Muhamad et al, 2016;Tomlinson, 2016;Duke, 2017).…”