plants Article Two Origins, Two Functions: The Discovery of Distinct Secretory Ducts Formed during the Primary and Secondary Growth in Kielmeyera Ellenhise R. Costa, Marcelo M. P. Tangerina , Marcelo J. P. Ferreira and Diego Demarco * Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo CEP 05508-090, Brazil; [email protected] (E.R.C.); [email protected] (M.M.P.T.); [email protected] (M.J.P.F.) * Correspondence: [email protected] Abstract: Secretory ducts have been reported for more than 50 families of vascular plants among primary and secondary tissues. A priori, all ducts of a plant are of the same type, and only slight variations in the concentration of their compounds have been reported for few species. However, two types of secretion were observed in primary and secondary tissues of Kielmeyera appariciana, leading us to investigate the possible influence of duct origins on the structure and metabolism of this gland. Kielmeyera appariciana has primary ducts in the cortex and pith and secondary ducts in the phloem. Both ducts are composed of uniseriate epithelium surrounded by a sheath and a lumen formed by a schizogenous process. Despite their similar structure and formation, the primary ducts produce resin, while the secondary ducts produce gum. This is the first report of two types of ducts in the same plant. The distinct origin of the ducts might be related to the metabolic alteration, which likely led to suppression of the biosynthetic pathway of terpenoids and phenolics in the secondary ducts. Citation: Costa, E.R.; Tangerina, M.M.P.; Ferreira, M.J.P.; Demarco, D. The functional and evolutionary implications of this innovation are discussed in our study and may Two Origins, Two Functions: The be related to the diversification of Kielmeyera and Calophyllaceae in tropical environments. Discovery of Distinct Secretory Ducts Formed during the Primary and Keywords: secretory ducts; structure; origin; resin; gum; evolution; Kielmeyera; Calophyllaceae Secondary Growth in Kielmeyera. Plants 2021, 10, 877. https:// doi.org/10.3390/plants10050877 1. Introduction Academic Editor: Elder Secretory ducts are internal glands composed of an epithelium formed by secretory Antônio Sousa Paiva cells that release the exudate in an elongated intercellular space called lumen [1]. They occur in 54 families of vascular plants, with a prevalence of resin ducts in 48 families [2,3] Received: 31 March 2021 and six families with mucilage ducts: Welwitschiaceae, Chloranthaceae, Combretaceae, Accepted: 23 April 2021 Malvaceae, Neuradaceae, and Vochysiaceae [4–8]. Secretory ducts are particularly common Published: 27 April 2021 in families, such as Anacardiaceae, Asteraceae, Burseraceae, Calophyllaceae, Clusiaceae, and Salicaceae, and some Fabaceae and Malvaceae [1,3,9–14]. Publisher’s Note: MDPI stays neutral Ducts may originate from ground meristem, procambium and/or cambium [1] and with regard to jurisdictional claims in published maps and institutional affil- vary from slightly elongated structures, as found in some Asteraceae, Malvaceae, and iations. Salicaceae [12,13,15], to extremely long, continuous ducts throughout the entire plant, as observed in conifers, Anacardiaceae, and Burseraceae [13]. Nevertheless, distinct secretory ducts within an organ in each species produce the same type of secretion in almost all plants, regardless of their origin [1,3,16]. While the secretion of the ducts has a variable composition in the species, they can be Copyright: © 2021 by the authors. generically grouped into three types: resin, mucilage, and gum [1,3,10], and each type of Licensee MDPI, Basel, Switzerland. secretion is usually conservative within the families [3,9], often being used as a diagnostic This article is an open access article distributed under the terms and character [17]. Few families have distinct genera producing different secretions in their conditions of the Creative Commons respective ducts, such as Anacardiaceae with resin ducts in almost all genera and gum ducts Attribution (CC BY) license (https:// in Lannea, Operculicarya, and Rhodosphaera [18,19]. Considering the resin ducts, only small creativecommons.org/licenses/by/ variations in the secretion composition have been observed comparing ducts of vegetative 4.0/). and reproductive organs in the same species, inferred from a different colour of the exudate Plants 2021, 10, 877. https://doi.org/10.3390/plants10050877 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 13 Plants 2021, 10, 877 2 of 13 only small variations in the secretion composition have been observed comparing ducts of vegetative and reproductive organs in the same species, inferred from a different colour of the exudate in each organ or based on the ultrastructure of the epithelial cells [20,21]. in each organ orDifferent based on types the of ultrastructure ducts occurring of the side epithelial by side have cells never [20,21 been]. Different reported types for Malpighiales of ducts occurringuntil sidenow. by However, side have our never field observations been reported remarkably for Malpighiales showed two until very now. distinct types However, our fieldof secretion observations being exuded remarkably by leaves showed and two stems very in distinctsecondary types growth of secretion in Kielmeyera appari- being exuded byciana leaves Saddi. and stems in secondary growth in Kielmeyera appariciana Saddi. Kielmeyera is oneKielmeyera of the largest is one generaof the largest of Calophyllaceae, genera of Calophyllaceae, comprising 50 comprising species, the 50 species, the leaf and bark extractsleaf and of bark which extracts are used of inwhich folk are medicine used in as folk anti-inflammatory, medicine as anti-inflammatory, antioxidant, antioxi- antibacterial, anddant, antifungal antibacterial, agents. and Recently, antifungal biological agents. assays Recently, have biological confirmed assays the efficacy have confirmed the of Kielmeyera extractsefficacyeven of Kielmeyera against carcinogenicextracts even cellagainst strains carcinogenic [22–24]. Thecell strains main secretion [22–24]. The main se- found in the genuscretion is resin,found whichin the genus is produced is resin, by which secretory is produced ducts located by secretory in all organs,ducts located in all mainly adjacentorgans, to the vascularmainly adjacent system to [9 ].the vascular system [9]. Secretory ductsSecretory occur in allducts species occur of in Calophyllaceae, all species of Calophyllaceae, and there are and divergences there are withdivergences with respect to theirrespect secretion, to their previously secretion, referred previously to as referred resin, gum, to as or resin, latex gum, [9,25 –or27 latex]. These [9,25–27]. These divergences raisedivergences doubts about raise the doubts type ofabout duct the present type of in duct the family present and in aboutthe family its possible and about its possi- diversity. Additionally,ble diversity. there Additionally, are still many there doubts are still in the many interpretation doubts in the of interpretation the anatomy of the anatomy these secretoryof structures these secretory as well structures as the chemical as well nature as the ofchemical the secreted nature compounds. of the secreted compounds. Therefore, we selectedTherefore,K. apparicianawe selectedas K. a modelappariciana to investigate as a model the to structure investigate of its the ducts structure of its occurring in primaryducts occurring shoots and in stemsprimary in shoots secondary and stems growth, in secondary the chemical growth, nature the of chemical their nature of exudate, as welltheir as theexudate, origin as of well these as ductsthe origin and of the these possible ducts influenceand the possible of their influence origin on of their origin their metabolism.on their metabolism. 2. Results 2. Results Kielmeyera apparicianaKielmeyerahas appariciana primary and has secondary primary and ducts secondary throughout ducts the throughout shoot system the shoot system (Figures1–3), which(Figures form 1–3), an which extensive form secretory an extensive network secretory that protectsnetwork allthat aerial protects parts all of aerial parts of the plant againstthe herbivory. plant against herbivory. Figure 1. Origin,Figure distribution, 1. Origin, distribution, and structure and of structure the primary of the resin primary ducts resin in Kielmeyera ducts in Kielmeyera appariciana appariciana. Astra blue. Astra and safranin staining. (A–D) Longitudinal sections. (E–G) Transverse section. (A) Origin of the primary resin ducts in cortex and pith blue and safranin staining. (A–D) Longitudinal sections. (E–G) Transverse section. (A) Origin of the of the shoot apex. (B) Strand of meristematic cells derived from ground meristem, which will form the duct lined by a primary resin ducts in cortex and pith of the shoot apex. (B) Strand of meristematic cells derived phenolic sheath (arrow). (C,D) Resin ducts in the parenchyma. Note the branched ducts formed by lateral fusion of two adjacent ducts.from ( groundE,F) Primary meristem, resin ducts which surrounded will form theby a duct phenolic lined sheath by a phenolic in the cortex sheath (E) (arrow).and pith ( FC).,D (G) Resin) Narrow resin ducts in theducts outer in cortex. the parenchyma. Arrowhead Note= resin the duct; branched DM = duct ducts meristematic formed by lateralcells; E fusion= epithelium; of two GM adjacent = ground ducts. meristem; Lu = lumen;(E ,PeF) = Primary periderm;