Laticifers in Sapindaceae: Structure, Evolution and Phylogenetic Importance

Abstract

Laticifer occurrence and structure are poorly known in Sapindaceae. Occurrence is likely underestimated owing to the low production of latex in most species. We investigated 67 species from 23 genera of Sapindaceae to verify laticifer occurrence and their structural, developmental and chemical features, as well as their evolutionary history in the family. Shoots were collected from herbarium and fresh specimens for histological analyses. Three characters derived from laticifer features were coded and their ancestral states reconstructed through Bayesian stochastic mapping and maximum likelihood estimation. Only articulated non-anastomosing laticifers were found in Sapindaceae. Laticifers differentiate early during shoot development and are found in the cortex, phloem, and pith. Latex is mostly composed of lipids. Callose and suberin were detected in laticifer cell walls in some genera. Reconstruction of laticifer ancestral states showed that laticifers are present in most clades of Sapindaceae with some reversals. Callose in the laticifer cell wall was found exclusively in Serjania and Paullinia (tribe Paullinieae), a character regarded as independently derived. Occurrence of laticifers in Sapindaceae is broader than previously reported. Articulated non-anastomosing laticifers had five independent origins in Sapindaceae with some secondary losses, occurring in five out of six genera of Paullinieae and 10 other genera outside Paullinieae. Particularly, callose in the laticifer cell wall evolved independently twice in the family, and its occurrence may be interpreted as a key-innovation that promoted the diversification of Paullinia and Serjania. Our study suggests that laticifer characters may be useful in understanding the generic relationships within the family.

Laticifer growth pattern is guided by cytoskeleton organization

“…Then, the daughter cell differentiates into a laticiferous cell whose terminal walls may be observed in the laticifer apex ( Milanez, 1960 , 1977 ; Gama et al, 2017 ). We observed that in the apical region, intercellular spaces are absent between laticifer and neighboring cells, corroborating observations from other studies ( Milanez, 1959 ; Demarco et al, 2006 ; Demarco and Castro, 2008 ; Medina et al, 2021 ). In particular, in the case of branched laticifers of Asclepias , where the laticifer cells can be a sinuous cylinder, they maintain the cell-to-cell wall adhesion with neighboring cells, contrary to the pattern observed in mesophyll cells, and the transverse arrangement of microtubules is uniform throughout the entire row of cells, not displaying differential growth or any different patterns that could promote polarized growth, as observed in unbranched laticifers.…”

“…Then, the daughter cell differentiates into a laticiferous cell whose terminal walls may be observed in the laticifer apex (Milanez, 1960(Milanez, , 1977Gama et al, 2017). We observed that in the apical region, intercellular spaces are absent between laticifer and neighboring cells, corroborating observations from other studies (Milanez, 1959;Demarco et al, 2006;Demarco and Castro, 2008;Medina et al, 2021). In particular, in the case of branched laticifers of Asclepias, where the laticifer cells can be a sinuous cylinder, they maintain the…”

“…This type of growth was described as symplastic growth by Fahn (1990). In particular, we observed that nonanastomosing laticifers can be longer and wider than the neighboring cells, which is probably related with differences in turgor pressure in the laticifer cells, which have a unique and distinct metabolism, and with their cell wall composition, as laticifer walls can be more acidic and thicker than neighboring cells in meristematic regions and also exhibit singular mechanical properties (Demarco et al, 2006;Palin and Geitmann, 2012;Demarco, 2015;Medina et al, 2021). The apical intrusive growth of internal cells might require neighboring cells forming intercellular spaces by detachment of middle lamella in order to intrusively grow between the spaces formed.…”

“…obs.) and (3) Urvillea ulmacea Kunth (Sapindaceae) with nonanastomosing laticifers ( Medina et al, 2021 ).…”

Two Origins, Two Functions: The Discovery of Distinct Secretory Ducts Formed during the Primary and Secondary Growth in Kielmeyera

“…There are rare reports of the presence of ducts in the primary phloem of some Clusiaceae and in the wood rays of Mammea (Calophyllaceae) and Garcinia (Clusiaceae) [ 2 , 3 , 9 ]. The occurrence of secretory structures only in primary tissues is common for some types of glands [ 1 ], but the occurrence of one type of secretory structure only in secondary tissues is extremely rare and has only been reported for laticifers of Hippocastanoideae (Sapindaceae) [ 30 ]. The other only report is the traumatic resin ducts of the wood of some conifers.…”