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Structure and distribution of articulated anastomosing laticifers in the shoots of Allamanda blanchetii. (A) Midrib of the leaf in transversal view. (B) Leaf blade in longitudinal view. (C) Transversal view of cortex and pith of stem, laticifers near the phloem. (D) Longitudinal view of a network of laticifers. (E) Colleter. Abbreviations: c ¼ cortex, p ¼ pith, ph ¼ phloem. Arrowhead ¼ laticifer, asterisk ¼ fusion of laticifers.
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Recent studies have shown the laticifers of Apocynaceae, previously classified as nonarticulated, indeed
are articulated, anastomosing laticifers whose transverse walls dissolve rapidly and entirely, although doubts about their growth mode still persist. To better understand the mode of laticifer growth and differentiation in this family, we studie...
Citations
... Laticifers are unicellular or multicellular structures distributed in primary and secondary plant structures that are highly specialized for latex synthesis (Fahn 1979;Mahlberg 1993;Teixeira et al. 2020;Oliveira et al. 2021;Marques et al. 2023). Laticifers originate in the cortex and pith ground meristem in the stem primary structure and are formed from vascular cambium derivatives in the secondary structure primarily located next to the sieve tube elements (Canaveze and Machado 2016;Gama et al. 2017;Souza et al. 2021;Salomé et al. 2023;Marques et al. 2023). ...
... Articulated laticifers can be nonanastomosed, when the walls of the precursor cells remain intact and form septate strips (Medina et al. 2021). The correct classification of laticifer structural type is only possible through ontogenetic studies, as the events that lead to their development occur very early in the apical meristem and cambium (Gama et al. 2017;Gonçalves et al. 2018;Teixeira et al. 2020;Souza et al. 2021;Salomé et al. 2023;Marques et al. 2023). ...
... Rights reserved. (Gama et al. 2017;Teixeira et al. 2020;Souza et al. 2021). The differentiation of laticifers in the stem apex occurs in a polarized and basipetal manner, originating from distal positions in the apical meristem and progressing basipetally towards more proximal positions (Gonçalves et al. 2018). ...
Laticifers are secretive structures with important roles in controlling abiotic and biotic stress through the external release of viscous and bioactive latex emulsions composed of alkaloids, terpenes, flavonoids, proteins, and mucilage. Allamanda cathartica is an attractive ornamental neotropical shrub that produces abundant latex with medicinal potential. The laticifers of this species, their origins, structural types, and distribution in the primary and secondary structures of the stem were investigated, and the chemical nature of latex was determined. Anatomical, histochemical, and ultrastructural evaluations of the stem apex were performed through light and electronic microscopy. Laticifers are abundant in the primary structure, being distributed in the cortex, outer primary phloem, and pith. Their branching, anastomosing structural type develops by the dissolution of the transverse and lateral walls of precursor meristematic cells, followed by protoplast fusion. The laticifers in the secondary structure are distributed amid the axial parenchyma cells of the phloem. The latex of A. cathartica is an emulsion composed mainly of mucilage and terpenes, and it is the first time that this laticifer system has been described.
... Also, the population of organelles found in the laticifer of H. lupulus seems to be strictly related to the chemical substances identified in its latex. Active dictyosomes are linked to polysaccharide production [1,56,57], and the extensive rough endoplasmic reticulum has a role in the phenolic production in the laticifer system [55,[58][59][60], both of which were observed in this study. The presence of many mitochondria with conspicuous cristae in actively developing laticifer systems generates a significant amount of ATP synthesis and may also serve other metabolic processes carried out by this secretory structure [58,61]. ...
... This observation aligns with the findings of this study, as fully developed laticifer cells of H. lupulus contain only latex products and a minimal peripheral cytoplasm. However, it is important to note that such subcellular machinery may not be applicable to all plant species, as some studies on articulated laticifer systems have shown diverse organelle compositions in their more developed stages, including the persistence of nuclei in specialized regions [44,60,70]. ...
Cannabaceae species garner attention in plant research due to their diverse secretory structures and pharmacological potential associated with the production of secondary metabolites. This study aims to update our understanding of the secretory system in Hops (Humulus lupulus L.), an economically important species especially known for its usage in beer production. For that, stems, leaves, roots, and inflorescences were collected and processed for external morphology, anatomical, histochemical, ultrastructural and cytochemical analyses of the secretory sites. Our findings reveal three types of secretory structures comprising the secretory machinery of Hops: laticifer, phenolic idioblasts and glandular trichomes. The laticifer system is articulated, anastomosing and unbranched, traversing all plant organs, except the roots. Phenolic idioblasts are widely dispersed throughout the leaves, roots and floral parts of the species. Glandular trichomes appear as two distinct morphological types: capitate (spherical head) and peltate (radial head) and are found mainly in foliar and floral parts. The often-mixed chemical composition in the secretory sites serves to shield the plant from excessive UVB radiation, elevated temperatures, and damage inflicted by herbivorous animals or pathogenic microorganisms. Besides the exudate from peltate glandular trichomes (lupulin glands), latex and idioblast content are also likely contributors to the pharmacological properties of different Hop varieties, given their extensive presence in the plant body.
... Latex exudation is observed throughout cross-sections of the stems in the primary structures of Apocynaceae species, as well as in the inner region of the bark in secondary structures (Gonçalves et al. 2018;Souza et al. 2021). Laticiferous ducts take on several structural forms that can be correctly identified only through ontogenetic studies of their precursor cells, with profound changes occurring early and over only short periods of time (Gama et al. 2017;Teixeira et al. 2020;Gonçalves et al. 2018;Almeida et al. 2021 Page 2 of 20 et al. 2021). Most of the laticifers described in Apocynaceae species are of the anastomosed type, in which adjacent cell walls dissolve to form a branched system of latex-secreting ducts (Lopes et al. 2009;Gama et al. 2017;Gonçalves et al. 2018;Souza et al. 2021); intrusive growth processes have also been reported, however, where cell ends elongate in the midst other surrounding meristematic cells (Canaveze and Machado 2016;Canaveze et al. 2018). ...
... Laticiferous ducts take on several structural forms that can be correctly identified only through ontogenetic studies of their precursor cells, with profound changes occurring early and over only short periods of time (Gama et al. 2017;Teixeira et al. 2020;Gonçalves et al. 2018;Almeida et al. 2021 Page 2 of 20 et al. 2021). Most of the laticifers described in Apocynaceae species are of the anastomosed type, in which adjacent cell walls dissolve to form a branched system of latex-secreting ducts (Lopes et al. 2009;Gama et al. 2017;Gonçalves et al. 2018;Souza et al. 2021); intrusive growth processes have also been reported, however, where cell ends elongate in the midst other surrounding meristematic cells (Canaveze and Machado 2016;Canaveze et al. 2018). Considering the wide diversity and geographic distribution of the Apocynaceae family, detailed studies of their laticifers will contribute to the expansion of knowledge concerning the complex ontogenesis of those secretory structures. ...
... The laticifers of M. zehntneri are structurally anastomosed and grow intrusively. For the correct identification of the structural type of a laticifer, their precursor cells must be examined among the meristematic cells at the elongating apex or among the meristematic cells derived from the vascular cambium (Gama et al. 2017;Gonçalves et al. 2018;Souza et al. 2021;Teixeira et al. 2020), Salomé et al 2022. Anastomosed articulated laticifers, as well as laticifers with intrusive growth originate, respectively, from the dissolution of adjacent cell walls or elongation through intercellular spaces (Fahn 1979;Malberg 1993;Johnson et al. 2021). ...
Main conclusion
Anastomosed laticifers with intrusive growth produce latex containing methyl comate and betulin with economic and ecological value in arid environments. Climatic factors influence laticifer development in the apical meristem and vascular cambium.
Abstract
Latex is a complex emulsion with high medicinal as well as ecological value related to plant survival. Marsdenia zehntneri is a shrubby plant that grows on limestone outcrops in the semiarid regions of Brazil. We sought to characterize the ontogenesis of the laticifers of this species and to relate that process to climatic seasonality and phenology through anatomical, ultrastructural, and micro-morphometric evaluations of the apical meristem and vascular cambium. The histochemistry of the secretory structure was investigated and the chemical composition of the latex was analyzed. Phenological assessments were performed by monitoring phenological events for 1 year. The laticifers network of M. zehntneri permeates the entire primary and secondary body of the plant, providing a wide distribution system of defensive compounds. Its laticifers, of a distinct mixed type (anastomosed, with intrusive growth), are numerous and voluminous in the apical meristem but scarce and minute in the secondary phloem. Latex secretion involves the participation of oleoplasts, polysomes, and dictyosomes. Methyl 2,3-dihydroxy-ursan-23-oate, methyl 3-hydroxy-ursan-23-oate, and betulin are encountered in high proportions in the latex and have ecological and medicinal functions. The development of primary laticifers is related to the resumption of apical meristem activity with increasing day length at the end of the austral winter. The development of secondary laticifers is related to high summer temperatures and rainfall that favor vascular cambium activity. The wide distribution of laticifers, their seasonal pattern of secretion, and their latex composition contribute to the adaptation of M. zehntneri to its natural environment.
... Although these general aspects of laticifer development Frontiers in Plant Science 02 frontiersin.org are well-known, how the laticifers grow is a question that is still postulated (Gama et al., 2017;Johnson et al., 2021). Two concurrent hypotheses based on observations from anatomical and developmental studies have been debated to explain their mode of growth in the plant body: (1) Laticifers grow through apical intrusive growth in meristematic regions, dissolving the middle lamella through enzymatic activity and growing intrusively between cells (Mahlberg, 1993;Canaveze and Machado, 2016;Castelblanque et al., 2016;Canaveze et al., 2019). ...
... (2) Laticifers may grow through the addition of new cells in the laticifer system followed by cell expansion, thus not through apical growth. Evidence supporting this view is the fact that laticifer apices (the region of the laticifer system where new cells that have just differentiated are added to the system) are found close to the shoot apical meristem but never penetrate this tissue (Milanez, 1960(Milanez, , 1977(Milanez, , 1978Demarco and Castro, 2008;Demarco et al., 2013;Gama et al., 2017;Ramos et al., 2019;Naidoo et al., 2020). ...
... However, laticifers may grow in a diverse mode, with ramifications and turns inside the plant body, which is difficult to follow and interpret using exclusively structural ontogenetic methodologies. The observation of an acute apex in some laticifers has frequently been interpreted as evidence that they have apical growth; however, the acute shape of the cell tip in the apical region of the laticifer may, in fact, be the result of an oblique section of the sinuous apical portion of the laticifers (Gama et al., 2017). Therefore, new approaches are required to assess this question. ...
Laticifers are secretory structures that produce latex, forming a specialized defense system against herbivory. Studies using anatomical approaches to investigate laticifer growth patterns have described their origin; however, their mode of growth, i.e., whether growth is intrusive or diffuse, remains unclear. Studies investigating how cytoskeleton filaments may influence laticifer shape establishment and growth patterns are lacking. In this study, we combined microtubule immunostaining and developmental anatomy to investigate the growth patterns in different types of laticifers. Standard anatomical methods were used to study laticifer development. Microtubules were labelled through immunolocalization of α-tubulin in three types of laticifers from three different plant species: nonanastomosing (Urvillea ulmacea), anastomosing unbranched with partial degradation of terminal cell walls (Ipomoea nil), and anastomosing branched laticifers with early and complete degradation of terminal cell walls (Asclepias curassavica). In both nonanastomosing and anastomosing laticifers, as well as in differentiating meristematic cells, parenchyma cells and idioblasts, microtubules were perpendicularly aligned to the cell growth axis. The analyses of laticifer microtubule orientation revealed an arrangement that corresponds to those cells that grow diffusely within the plant body. Nonanastomosing and anastomosing laticifers, branched or not, have a pattern which indicates diffuse growth. This innovative study on secretory structures represents a major advance in the knowledge of laticifers and their growth mode.
... The discontinuity of transverse cell walls associated to cell accumulation in protoplast is responsible of laticiferous cell creation [24,26]. Latex secretion implies protoplasm degeneration, restriction of the cytoplasm, and fusion of small vacuoles with some vesicles into the central vacuole [27]. ...
... In leaves, laticifers were scattered in the mesophyll (spongy and palisade) and localised also in the central cylinder ( Figure 3). Obtained results were in accordance to those found previously for other Asclepiadaceae [12,27,36,38]. While in other study, secretory cells were found towards leaf extremities [26]. ...
Pergularia tomentosa is a perennial twining herb widely spread out arid and semiarid Tunisian regions. It is searched for its richness in enzymes, secondary metabolites, antifungal activity, and milk-clotting activity. Traditional use implies the fresh latex in wounding heals. The present study was aimed at identifying laticifer distribution in Pergularia tomentosa stems, leaves, and petioles. In the present study, the identification of latex extract’s components and its valorisation by estimation of phenolic content, flavonoids, and antioxidant activity are conducted. Anatomical structures proved the presence of laticifers in the aerial parts of Pergularia tomentosa. They are particularly observed along the pith and cortical parenchyma in stem, in leaf mesophyll, and in petiole phloem. Identified laticifers were characterized as nonarticulated. FTIR spectroscopy proves the presence of several functional groups in the latex and mainly the cis-1-4-isoprene monomer. Results suggested that Pergularia tomentosa latex contributes significantly as a source of phenol content (62.3 mg Eq GAE/g) and flavonoids (24.8 mg Eq QE/g). Scavenging free radicals of DPPH exhibited IC50 value of 12 μg/ml. In conclusion, latex extracted from Pergularia tomentosa can be implied in industry as a natural rubber. It can be used, also, in medicine as a therapeutic agent.
... The Apocynaceae family comprises many latex-producing species, and the anastomosing structural type of laticifer is reported to be predominant in the group (Gama et al. 2017;Pirolla-Souza et al. 2019). Laticifers of this type are formed by rows of cells whose terminal and lateral walls are absorbed, forming elongated and branching ducts (Gonçalves et al. 2018;Souza et al. 2021). ...
... Ontogenetic studies that allow a complete definition of the anastomosis processes through dissolution of adjacent cell walls are required for Handling Editor: Alexander Schulz. the correct definition of their structural type (Gama et al. 2017;Gonçalves et al. 2018;Teixeira et al. 2020;Souza et al. 2021). ...
... In C. procera the presence of laticifer is recorded in the cortex, pith, and between the outer and inner phloem strands of the bicollateral bundles of the stems. In Allamanda blanchetii (Gama et al. 2017), laticifer was recorded in the cortex and medulla and in the inner primary phloem. Pro-cambial origins were recorded in Tabernaemontana catharinensis (Canaveze and Machado 2016), and Vallaris solanaceae (Gondaliya and Rajput 2016). ...
An in-depth understanding of the development and distribution of laticifer (latex secretory structure) will be important for the production of both rubber and medicines and will support studies on plant adaptations to their environments. We characterize here and describe the ontogenesis of the laticifer sytem in Calotropis procera (Apocynaceae), an invasive subshrub species in arid landscapes. Anatomical and histochemical evaluations of the primary and secondary structures of the stem were carried out on a monthly basis during a full year, with ultrastructural evaluations of laticifer on the stem apex during the rainy season. In the primary structure, laticifer differentiate early from procambium and ground meristem cells of the cortex and medulla and become concentrated adjacent to the external and internal phloem of the bicollateral bundles. In the secondary structure, laticifer differentiates from fusiform derivative cells of the phloem close to the sieve-tube elements. The laticifer is of the articulated, anastomosing, branched type, and it originates from precursor cells that loose the transversal and longitudinal walls by dissolution. Latex is a mixture of terpenes, alkaloids, flavonoids, mucilage, and proteins. The apical meristem and vascular cambium where the laticifer system begins its development are active throughout the year, including during the dry season. The vascular cambium produces phloem with laticifer precursor cells during the rainy season, with high temperatures and long days. The ability of C. procera to grow under water deficit conditions and produce laticifer throughout the year contribute to its wide distribution in arid environments.
... To date, there have been no subcellular studies of laticifers of Sapindaceae. However, considering the fact that laticifers of the family produce lattices with similar classes of compounds to those of other families (Ramos et al. 2020), we can predict that laticifers in Sapindaceae should have a dense cytoplasm with many secretory vesicles formed by endoplasmic reticulum and plastids, numerous mitochondria, and abundant lipid bodies distributed throughout peripheral and central vacuole Mahlberg 1978, 1980;Inamdar et al. 1988;Roy and De 1992;Gama et al. 2017;Fang et al. 2019). The central vacuole is the most (Medina et al. 2021). ...
Sapindales comprise nine families with a mainly tropical distribution and include numerous species of high economic importance. Members of this order are known for the production of chemical constituents with medicinal properties, such as antioxidant, anti-inflammatory, and antimicrobial activity, as well as species with insecticidal properties. Such diversity of chemical compounds is attributed to a variety of secretory structures, which may occur in both vegetative and reproductive organs. During the past decades, tremendous progress has been made in anatomical and analytical chemistry studies, which has led to the next level of knowledge regarding the secretory structures of Sapindales. This comprehensive review embraces the most important data of the secretory structures of Sapindales: ducts, cavities, laticifers, floral and extrafloral nectaries, osmophores, colleters, idioblasts, and trichomes. Our review comprises structural, functional, and evolutionary aspects of these glands, which are fundamental for further studies of the diversification within Sapindales.
... To date, there have been no subcellular studies of laticifers of Sapindaceae. However, considering the fact that laticifers of the family produce lattices with similar classes of compounds to those of other families (Ramos et al. 2020), we can predict that laticifers in Sapindaceae should have a dense cytoplasm with many secretory vesicles formed by endoplasmic reticulum and plastids, numerous mitochondria, and abundant lipid bodies distributed throughout peripheral and central vacuole Mahlberg 1978, 1980;Inamdar et al. 1988;Roy and De 1992;Gama et al. 2017;Fang et al. 2019). The central vacuole is the most (Medina et al. 2021). ...
... But laticifers and idioblasts were not observed in leaves of W. tinctoria. Generally, laticifers of most species of Apocynaceae are considered to be non-articulated (Gama et al., 2017), and Seenu et al. (2019) reported the presence of non-articulated laticifers in the leaves of T. alternifolia. In the present study, sclerenchymatous tissues were observed in leaves of both the Wrightia species as noted in the leaves of W. candolli by Hernandez et al. (2019), and these tissues were shown to play a role in preventing excessive transpiration to some extent and also provide mechanical support to the leaves. ...
Wrightia tinctoria R.Br. and the endemic Wrightia indica Nagn are important medicinal plants possessing novel therapeutic compounds. However, the anatomy of these medicinal plants is not well studied. Therefore, the present study illustrates the vegetative anatomy of the two Wrightia R.Br. species using light microscopy. The stomata in the leaves were paracytic/anomocytic type in W. tinctoria and of paracytic type in W. indica. The foliar cuticle was of varying thickness, and multicellular trichomes were distributed on the abaxial surface of W. tinctoria and both leaf surfaces of W. indica. The leaf anatomical characters like uniseriate epidermis, collenchymatous hypodermis, heterogeneous mesophyll, endarch xylem, idioblasts, starch grains, and raphides were common for both the Wrightia species. Stems of W. indica were sparingly covered by multicellular trichomes. The stems of both Wrightia species possess uniseriate epidermis, angular collenchymatous hypodermis, parenchymatous cortex, starch grains, bicollateral vascular bundles with endarch xylem, idioblasts containing calcium oxalate crystals and water-cells in the stelar region. Starch grains were abundant in the pith of W. indica. The root periderm consists of rectangular cells and the cortex was parenchymatous in both Wrightia species. Water-cells and sclereids were present in the cortex of W. tinctoria, whereas sclereids were absent in W. indica. Vascular bundles were amphicribral in both Wrightia species. Significant differences were evident in the cellular dimensions of vegetative parts of both the Wrightia species. The observations of the present study indicate that the vegetative anatomy could aid in the discrimination of these two Wrightia species.
... They can originate from the promeristem in the primary plant body (Gonçalves et al. 2018) and from the vascular cambium, especially from the phloem initials in the secondary structure Leme et al. 2020;Pace et al. 2019;Rao et al. 2013;Tan et al. 2017). Latex represents a suspension composed of both hydrophilic and lipophilic compounds and maintained under pressure in the laticifers (Gama et al. 2017; Communicated by B. Fernandez-Marin. Trees and Teixeira 2019; Naidoo et al. 2020). ...
... The non-anastomosed type with intrusive growth has been reported in T. catharinensis (Canaveze et al. 2019) and in other various species of the family (Hagel et al. 2008;Teixeira et al. 2020). The process of cell wall lysis, which leads to anastomosis and the ontogenesis of laticiferous ducts, occurs very early and can be confused with cells elongated by intrusive growth (Gama et al. 2017;Gonçalves et al. 2018;Teixeira et al. 2020). Thus, ontogenetic studies are necessary for their correct classification. ...
... The branched laticifers in the primary stem structure of H. speciosa are distributed in the cortex and pith and differentiate early from the ground meristem. That distribution pattern is common in Apocynaceae (Lopes et al. 2009;Krentkowski and Duarte 2012;Canaveze and Machado 2016;Gama et al. 2017;Pirolla-Souza et al. 2019;Naidoo et al. 2020) and families such as Euphorbiaceae (Kumar et al. 2012;Rajeswari et al. 2013), Malpighiaceae (Pace et al. 2019), and Cannabaceae ). ...
Key message
In Hancornia speciosa, the latex is synthesized in the cytosol of the ground meristem cells and in plastids of the fusiform derivatives of secondary phloem. Laticifer development is related to climatic seasonality.
Hancornia speciosa is a latescent species that grows in the Brazilian Cerrado (neotropical savanna) and shows significant potential for rubber production and the extraction of bioactive compounds from its latex. We examined the development of laticifers in its stem apex and secondary phloem in relation to climate seasonality. Morphometric evaluations of elongating branches and micromorphometric evaluations of the cambial zone were carried out monthly for 1 year, with structural and ultrastructural analyses of the stem apex and secondary phloem. Laticifer development in both the stem apex and secondary phloem is related to increasing day length and maximum temperature and humidity. Laticifers are formed by anastomosis of the transverse and longitudinal walls of the ground meristem cells of the stem apex, and the fusiform derivatives of secondary phloem in the cambial zone. The process of latex secretion involves the synthesis of terpenic droplets in the cytoplasm of the ground meristem cells of the stem apex and in the plastids of the fusiform derivatives of secondary phloem. Latex is an emulsion formed by the cytosol terpenic droplets engulfed by vacuoles contaning mucilages and proteins secreted by dictyosomes and rough endoplasmic reticulum, and alkaloids secreted by the phloem cells. This work expands our knowledge concerning the development of laticifers in Apocynaceae and contributes to our better understanding of the influence of environmental factors on latex secretion.
