Structures and functions of adventitious roots in species of the genus Philodendron Schott (Araceae)

Flora 209 (2014) 547–555

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Structures and functions of adventitious roots in species of the genus Philodendron Schott (Araceae)夽 Vitor Tenorio ∗ , Cassia Mônica Sakuragui, Ricardo Cardoso Vieira Federal University of Rio de Janeiro, Institute of Biology, Department of Botany. Vegetable Morphology Laboratory. Av. Brigadeiro Trompowsky, Cidade Universitária, Ilha do Fundão, 21941590, Rio de Janeiro, RJ, Brazil

a r t i c l e

i n f o

Article history: Received 5 September 2013 Accepted 20 July 2014 Edited by Dr. Rainer Lösch. Available online 12 August 2014 Keywords: Root anatomy Root dimorphism Adaptation Stele

a b s t r a c t We discuss here the anatomical variations of the arrangements and compositions of stele types observed in different roots types in four populations of the three species of Philodendron as probable adaptations to their habitats. Terrestrial individuals of P. corcovadense have cylindrical steles while rupicolous individuals have lobate steles with dispersed internal cortical parenchyma. The Philodendron species sampled showed polyarch structures. The crampon roots of P. oblongum and anchor roots of P. cordatum show medullated protosteles, with the former species having a reduced pith with sclerified parenchyma cells while the latter has a wide pith and parenchyma cells with only slightly thickened walls. The feeder roots of P. cordatum also show a medullated protostele—although a central vessel is present until approximately 60 cm from the apex that later disappears, forming a parenchymatous pith. We conclude that the different root types reflect adaptations of the subgenera Philodendron and Meconostigma to their different habits and habitats, such as in P. corcovadense, where the roots of rupicolous individuals have lobate steles while the roots of the terrestrial plants have cylindrical steles. © 2014 Elsevier GmbH. All rights reserved.

Introduction Philodendron is the second largest genus of the family Araceae, with nearly 400 species (Govaerts and Frodin, 2002) although future investigations may expand this number to approximately 700 species (Croat, 1997). It is a morphologically and ecologically diverse neotropical genus occurring from northern Mexico to southern Uruguay (Mayo et al., 1997), being very abundant in tropical rain forest habitats (Sakuragui, 2001). One hundred and fifty-six species of Philodendron have been described from Brazil (Sakuragui and Soares, 2010) that predominantly grow in humid tropical forests, but are also found on rock outcrops and in swamps, riparian forests, and semiarid regions. According to Benzing (1987), 20–25,000 species of vascular epiphytes occur in the tropics, with 80% of all epiphyte species being monocots. Epiphytes are largely encountered in tropical rain forests (Kress, 1989) and are partially responsible for the great diversities found in those complex terrestrial ecosystems (Gentry and Dodson, 1987). Rupicolous species develop in environments with high solar

夽 Part of the Master’s dissertation of the first author. ∗ Corresponding author. E-mail address: [email protected] (V. Tenorio). http://dx.doi.org/10.1016/j.flora.2014.08.001 0367-2530/© 2014 Elsevier GmbH. All rights reserved.

radiation and wide temperature variations and can be exposed to strong winds and to water stress (Burke, 2002). Philodendron taxa grow in a wide variety of habitats as terrestrial, epiphytic, rupicolous, or hemiepiphytic plants. Hemiepiphytic individuals have epiphytic and terrestrial stages in their life cycles, with, prior to living as hemiepiphytes, germinating and initially growing as epiphytes. After germination and initial development on host trees these plants later develop aerial roots that grow toward the ground. But Aroids are usually classified as secondary hemiepiphytes, as they germinate as terrestrials and then develop ˜ et al., 1999). aerial roots that attach them to the host tree (Patino According to Zotz (2013), however, the use of the term “secondary hemiepiphyte” should be discontinued in favor of using term “nomadic vine” (for details see Zotz, 2013). Due to the wide variety of adventitious root types in the Araceae family, a dimorphism related to their function as feeder roots (which absorb water and nutrients from the substrate) and anchor roots (which attach the plants to their hosts) can be observed. Feeder and anchor roots show morphological and physiological differences (French, 1997), and Mayo (1991) illustrated root dimorphism in Meconostigma. Two subgenera were recognized in the revision of the genus by Krause (1913): Euphilodendron (=Philodendron) and Meconostigma. Subsequent analysis of anatomical characters led Mayo (1989) to elevate the section Pteromischum (subgenera Philodendron) to the

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Table 1 Specimens used in this study and the root types of each one.

Species Subgenus Habit Biome Root type Voucher

Population A

Population B

Population C

Population D

P. corcovadense Kunth Meconostigma Terrestrial Atlantic forest Feeder RFA 37317

P. corcovadense Kunth Meconostigma Rupicolous Atlantic forest Anchor and feeder RFA 37490

P. cordatum Kunth ex Schott Philodendron Nomadic vine Atlantic forest Anchor and feeder RFA 37309

P. oblongum Kunth Pteromischum Epiphyte Amazon, Atlantic forest Crampon RFA 37319

subgenus rank, so that three subgenera (Pteromischum with 75 species, Meconostigma with 20 species, and Philodendron with over 250 species) are now currently accepted (Mayo et al., 1997). The root vascular plexus represents the connections between adventitious roots and the vascular system of the stem (French and Tomlinson, 1984). The subgenera Philodendron and Meconostigma have a vascular plexus formed by branched vascular bundles while the vascular plexus of Pteromischum species is composed of simple vascular bundles. This feature is related to the diversification of the habits and habitats of the subgenera, and a branched vascular plexus is a synapomorphy of the monophyletic clade comprising the subgenera Philodendron and Meconostigma (Tenorio et al., 2012)—and the presence of this branched vascular plexus possibly led to the occurrence of root dimorphism in these subgenera. Assuming that variations in Philodendron root types occurred due to the vascular plexus, the objective of this work was to anatomically describe the different root types and identify adaptations to their habitats and their links to anatomical variations among the different root types. Materials and methods Three individuals from four populations each (representing three different species) were examined in the anatomical analyses: population A (terrestrial) and population B (rupicolous) of Philodendron corcovadense, population C (hemiepiphyte) of P. cordatum, and population D (nomadic vines) of P. oblongum, all from areas of Atlantic Forest in Rio de Janeiro State, Brazil (Table 1). Voucher specimens were deposited in the Herbarium of the Federal University of Rio de Janeiro (RFA). The samples were fixed in FPA (50 mL of 95% ethyl alcohol; 5 mL propionic acid; 10 mL formaldehyde, and 35 mL distilled water) (Ruzin, 1999) and stored in 70% ethanol (Johansen, 1940). Anatomical studies were performed using light microscopy. Root samples were processed using the traditional method of PEG embedding (Burger and Richter, 1991). Transverse sections (15–20 ␮m thick) were prepared using a rotary microtome, stained with safranin and astra blue dye (Bukatsch, 1972), and mounted in Canada balsam. Average values of the diameters of the root metaxylem and metaphloem were obtained from 30 measurements of each individual collected. Maximum, minimum, and average values are recorded here, as well as the standard deviations of each character. Results The adventitious roots of the species analyzed all emerge from the aerial nodal regions of the stems. Philodendron corcovadense was represented by a population of terrestrial individuals with adventitious roots—classified here as feeder roots—(Fig. 1A) and by another population of rupicolous individuals with adventitious anchor–feeder roots which initially support the individuals on rocks and then detach, growing toward the substratum and assuming the role of feeders (Fig. 1B). The roots of the hemiepiphyte P. cordatum (Fig. 1C) analyzed were anchor roots (with a fastening function) as well as feeder roots (whose function is to absorb

water and nutrients). The nomadic vine P. oblongum has roots of the crampon type (Fig. 1D and E). The anchor roots of P. corcovadense and P. cordatum were approximately 100 cm long and reddish brown or light brown, becoming more orange tinted near the apex; the feeder roots were approximately 2 m long and showed a welldeveloped system of lateral roots. The crampon roots of P. oblongum were approximately 5–8 cm long, with smaller diameters and a brownish coloration. During growth, the epidermis and exodermis of P. corcovadense and P. cordatum are gradually discarded and substituted by a storied cork layer through continuous periclinal divisions of the cortical parenchyma (Fig. 2A–C). The crampon roots of P. oblongum showed a uniseriate epidermis and exodermis, with the latter being sclerified (Fig. 2D). Root hairs could be observed on P. oblongum. The exodermis cells are uniform in all of the species investigated, with similar shapes and sizes. The cortexes of all of the species can be divided into internal, median, and external layers. The cortex of the mature root of P. corcovadense shows loosely arranged cells (Fig. 2E) while the anchor and feeder roots of P. cordatum and the crampon roots of P. oblongum have compact cortexes with few intercellular spaces (Fig. 2G). The external cortex P. oblongum is composed of approximately 13 cell layers with lignified walls (Fig. 2D). The roots of all of the species studied here show resiniferous ducts distributed throughout the cortex, forming various numbers of rings among the different species. Approximately two rings were observed in P. corcovadense, (Fig. 2E) while P. cordatum has approximately 7 rings of ducts throughout the cortex (Fig. 2F); only 1–2 rings were observed in P. oblongum (Fig. 2H). The resin ducts are of schizogenic origin, as their lumens are formed by the division and separation of cortical parenchymatous cells (Fig. 2H). P. corcovadense has 2–3 layers of thin-walled parenchymatous cells surrounding the epithelial layer of the resin duct. The resiniferous ducts of P. cordatum and P. oblongum are surrounded by a sclerified sheath, with approximately 3–5 cell layers surrounding the epithelial layer (Fig. 2F and G). The ducts of P. cordatum in the external cortex did not appear to have sclerified sheaths (Fig. 2C). The endodermis layers of all examined species are uniseriate and have visible Casparian strips (Fig. 3A and B). P. corcovadense retains the Casparian strips even in mature roots while the endodermis of mature roots of P. cordatum and P. oblongum attains stages of greater differentiation—with depositions of lignin/suberin that give the cell walls an O-shaped appearances in microscopic cross sections. The anchor and feeder roots of P. cordatum show strong sclerification of the more internal cortical layers at later stages, with greater differentiation (Fig. 3C–F). The vascular cylinders of the investigated roots frequently showed phloem strands surrounded by cells with highly lignified walls. However, the cells that surround the phloem strands of P. corcovadense, retain their thin primary walls (Fig. 3A). In P. cordatum and P. oblongum such cells extend to regions of pericycle and endodermis which are external to the phloem strands (Figs. 3C and D). The phloem strands in P. corcovadense and P. cordatum roots appear short or long in cross section, depending on their respective radial

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Fig. 1. A–E. Species of Philodendron examined in the present study. A: P. corcovadense, terrestrial individual; B: P. corcovadense, rupicolous individual; C: P. cordatum, nomadic vine; D and E. P. oblongum, epiphyte. Note the crampon roots in E.

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Fig. 2. A–H. Transversal sections of the adventitious roots. Storied cork formations in the roots of P. corcovadense (A and B) and P. cordatum (C). Note the collapsed epidermis, and pluriseriate and lignified exodermis (A) and cells in periclinal division giving origin to a stratified suber (A and B). C: Detail of the exodermis and periclinal divisions (arrow) in the feeder root of P. cordatum. D: Root of P. oblongum showing the epidermis dotted with trichomes, sclerified exodermis, and cortical cells with lignified cell walls. E, F, G: Distribution of resiniferous ducts. Root of P. corcovadense (E). Note the distribution of the ducts (arrows) in 2 rings surrounding the cortex. Anchor root of P. cordatum (F). Note the distribution of resiniferous ducts throughout the cortex (arrows). Root of P. oblongum (G). Note the resiniferous ducts (arrows) distributed in a single ring. H: P. corcovadense, detail of a resiniferous duct, demonstrating its schizogenic origin. Ep (epidermis); Ex (exodermis); Sto (stratified suber); Ec (external cortex). Bars = 51 ␮m (A), 63 ␮m (B), 61 ␮m (C), 10 ␮m (D), 67 ␮m (E), 34 ␮m (F), 37 ␮m (G), 170 ␮m (H).

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Fig. 3. A–F. Transversal sections of adventitious roots, showing the contacts between the cortex and central cylinder. A: P. corcovadense, pericycle, endodermis, and vascular elements. B, C: Anchor root of P. cordatum. Casparian strips (arrows) in polarized light (B). Note the internal cortex, endodermis, and sclerified pericycle (arrow) (C). D: Feeder root of P. cordatum. Note the vascular elements. Arrows indicate the protoxylem. E, F: Root of P. oblongum. Sclerification around the phloem strands (arrows) can be seen under polarized light (E) and the vascular elements only (F). Ph (phloem); Lp (long phloem strands); Sp (short phloem strands); Mx (metaxylem); Px (protoxylem); End (endodermis). Bar = 46 ␮m (A), 23 ␮m (B), 10 ␮m (C and D), 27 ␮m (E), 34 ␮m (F).

extensions (Fig. 3A, C, and D). The phloem strands of the feeder roots of P. cordatum are longer than those of the anchor roots (Fig. 3C and D) while the phloem strands of P. oblongum are consistently rather short (Fig. 3F).

All Philodendron species studied here show polyarch structures in transverse sections. The crampon roots of P. oblongum and the anchor roots of P. cordatum have medullated protosteles, with the former species having a reduced pith with sclerified parenchyma

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Fig. 4. A–F. Transversal sections of adventitious roots showing the vascular cylinder. A: P. corcovadense feeder root. Note the cylindrical shape of the stele, with metaphloem dispersed throughout the xylematic mass (arrows). B: Anchor/feeder root of P. corcovadense. Lobate stele, although the vascularization pattern is similar to that of a feeder root. C, D: Crampon root of P. oblongum (C), and anchor root of P. cordatum (D). Note the medullated protostele. E, F: Feeder root of P. cordatum showing the development of a vascular cylinder of the protostelic type. Note the metaxylem in the center of the stele (arrow), not occurring in the differentiated root (F). Note the differences in densities and diameters between the different root types of P. cordatum (D and F). Mx (metaxylem); Mf (metaphloem); Me (medulla). Bar = 10 ␮m (A, C and D), 20 ␮m (B and E), 460 ␮m (F).

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Table 2 Mean values (minimum–maximum) ± standard deviation of metaxylem (MX) and metaphloem (MF) diameter (in ␮m) for each type of root of the studied Philodendron species. Species

Habit

Root type

MX

MF

P. cordatum

Nomadic vine

P. oblongum P. corcovadense

Epiphyte Terrestrial Rupicolous

Feeder Anchor Crampon Feeder Anchor/feeder

177(131.9–203.7) ± 21.6 106 (92–123.4) ± 11.2 28 (24.2–31.4) ± 2.2 100 (90.5–112.2) ± 6 92.5 (82.3–103.5) ± 6

42 (32.9–49.6) ± 5.4 27.5 (21.4–34.3) ± 4.1 5.9 (4.3–7) ± 0.8 36.5 (33.6–39.4) ± 2.5 31.5 (26.6–38.7) ± 3.4

cells while the latter shows a wide pith and parenchyma cells with slightly thickened walls (Fig. 4A and B). The feeder roots of P. cordatum also possess medullated protosteles although a central vessel could be observed until approximately 60 cm from the apex. This structure would later disappear, giving way to the formation of a narrow pith (Fig. 4C and D). P. corcovadense showed a protostelic type in both populations, with elements of the metaphloem being distributed throughout the xylem cross-sectional area (Fig. 4E and F). The feeder roots of P. corcovadense have cylindrical steles (Fig. 4E) while rupicolous P. corcovadense plants have lobate steles (Fig. 4F), with the internal cortical parenchyma intruding into them (Fig. 4F). The anatomy of P. corcovadense generally has a somewhat intermediate character, with the distribution of vascular elements being characteristic of feeder roots (with the metaphloem inserted into the xylem tissue), whereas the diameters of the vascular elements themselves are more similar to those of anchor roots, i.e., smaller than typical feeder roots (Table 2). Discussion In a study of the anatomy of the adventitious roots of the Araceae family, French (1987a, 1987b) emphasized the occurrence of a sclerified hypodermis and resiniferous channels as well as the systematic implications of those structures. Vianna et al. (2001) studied the anchor roots of Philodendron bipinnatifidum (which have lobate steles) while Hinchee (1981) conducted studies on the different types of roots of Monstera deliciosa, classifying them as aerial, aerial–subterranean, or lateral subterranean. These studies demonstrated various important anatomical characteristics that can be observed in Araceae roots. French and Tomlinson (1984) reported that the root vascular plexus is a transitional connective region between the stem and the root, and Tenorio et al. (2012) reported that the bundles in this region can be branched or simple, as seen in cross section. The investigated species P. corcovadense and P. cordatum belong to the subgenera Meconostigma and Philodendron, respectively, P. oblongum belongs to Pteromischum. According to Tenorio et al. (2012), the subgenera Meconostigma and Philodendron have branched vascular plexuses, and this character possibly may have led to a major diversification, both of their habits and of the habitats they could occupy. Thus the occurrence of different root types in species of these subgenera can reflect their adaptations to different environmental conditions, and present results indicate that the species growing in different environments indeed show significant differences in the compositions of their steles. Such differences first of all exist between the diameters of the different root types. The feeder roots of Philodendron cordatum have the greatest average diameters of their vascular elements, which may indicate that they are well adapted to the absorption and conduction of water and nutrients. The anchor roots of the same species, however, have vascular elements with considerably smaller diameters—which reflect the different functions of the two root types. Similar differences were also observed in the different roots of P. corcovadense plants that grow either terrestrially or on rocky outcrops. According to Tomlinson and Fisher (2000), vessel

elements with wide diameters serve for water storage and its rapid transportation. P. oblongum had the smallest average metaxylem and metaphloem diameters in the present study, reflecting their primarily crampon-like fastening function. According to Carlquist (1975), vessel distributions in monocot axes should be understood as different aspects of their conduction characteristics in different organs within the same plant. The feeder roots of P. cordatum have larger vessel diameters and densities than the anchor roots, and the feeder roots have a vessel in the center of the stele, which is absent in anchor roots. The anatomical differences between the vessels of these two root types can be taken as a further proof of Carlquist’s statement (1975) that different conductivity characteristics lead to differences in the distribution and structure of vessels in different root types, even in the same individual. The shapes of the vascular cylinders in P. corcovadense differed among the different roots types in the populations analyzed. Roots of other Philodendron taxa belonging to the subgenus Meconostigma have lobate steles, and this was observed in rupicolous individuals of P. corcovadense, too. However, the roots of these plants must not necessarily function as anchor roots simply because they have a stellar outline typical for this functional root type. The significance of this character still must be analyzed further, keeping in mind that it has only been found in Meconostigma species within the genus Philodendron and may be a primarily taxonomy-related trait. Mayo (1991) reported that lobate steles are also present in the genus Cercestis—a genus close to Philodendron, and both genera are included in the Homalomena clade, according to Cusimano et al. (2011). In terms of the functional aspect of the lobate stele, further it must be kept in mind that the adventitious roots of rupicolous individuals of P. corcovadense first anchor the plant to the rocks, but detach later to become feeders although these roots probably absorb rain water also in the anchor phase. However, the largest quantities of water and nutrients are probably absorbed from the soil substrate—and it is quite plausible in this sense that the anatomy of these roots lies between anchor and feeder root types. The interlocking placement of cortical parenchyma and stelar tissue (leading to the lobate aspect of the roots in cross section) may increase the efficiency of water absorption and conduction by increasing the lateral surface area of the stele while still maintaining an appropriate mechanical stiffness and flexibility. The adventitious roots of the Philodendron species investigated here all originate from the stem in nodal regions, but differ in their functions—either tapping the soil to absorb water and nutrients or providing support to the rupicolous plants respectively those that are growing as nomadic vines. French (1997) denominated the roots of epiphyte and hemiepiphyte (nomadic vine) plants with support functions as anchor roots, and considered as feeder roots all those that are extending to the soil to absorb water and nutrients. However, Philodendron taxa, and the Araceae in general, are somewhat peculiar in this sense, since they can initiate their life cycles as terrestrial plants, developing only later anchor roots (crampon or not) that are bound to support structures (usually tree trunks), and growing upward into the canopy region toward better

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light conditions. Ball et al. (1991) underlined that epiphytism (where access to light is not a primary problem) can considerably diminish access to nutrients and water. The root structures of these different life forms (including one genus investigated in the present study) do, in fact, represent different strategies coping with shortage of different resources. The dimorphism of the adventitious roots of Philodendron cordatum—with greater feeder root diameters and densities as compared to anchor roots—shows a way, how this nomadic vine can maintain itself both on the phorophyte and the soil, getting sufficient access to both, the soil and the atmospheric resources. No strict dimorphism was observed in the two P. corcovadense populations analyzed here, but rather anatomical differences between the terrestrial and rupicolous populations. The anchor roots of the crampon type in P. oblongum, finally, are completely adapted to the epiphytic habitat of that species. Root hairs were observed in all species although in the epiphyte P. oblongum they are only present on the mature roots. The presence of a pluristratified epidermis (velamen) composed of dead cells can be observed on aerial roots of epiphytic plants in the families Bromeliaceae and Araceae (Pita and Menezes, 2002), described, e.g., in detail in Philodendron appendiculatum (Sakuragui, 1998), and are very well known from many members of the Orchidaceae (Bona et al., 2004). The velamen serves to reduce water loss, provides mechanical protection, and increases water absorpt. In the epiphyte P. oblongum, no distinct velamen was observed, but its root hairs and the sclerified exodermis apparently contribute preventing retarding desiccation of the atmosphere-exposed roots. Hose et al. (2001) described the exodermis as a hypodermal layer with Casparian strips, and Cutter (1987) and Dickison (2000) defined it as a type of hypodermis typical of certain roots that may or may not be suberized or lignified, or even contain Casparian strips. Beck (2005) characterized cell strata with lignified walls just below the exodermis as a hypodermis that can be found on the roots of many herbaceous dicotyledonous and monocotyledonous plants, as well as in certain palm trees. French (1987b) described a sclerified hypodermis to occur in eight genera of Araceae (including Philodendron) and distinguished it from the exodermis, mainly on the basis of morphological characteristics—including cell size and the thickness of the cell wall. In present study we called all subepidermal layers as exodermis tissues. Where proximal lignified cell layers, below the exodermis, were present (such as in P. oblongum) they were treated as part of the cortex, considering the exodermis as a special type of root hypodermis. The resiniferous ducts observed in the studied species are of schizogenic origin, as it was described also by Vianna et al. (2001) for the anchor roots of Philodendron bipinnatifidum. The origin of such ducts was described by Beck (2005) and Evert (2006) as a separation of cells from each other, resulting in a central space lined by an epithelium of secretory cells. In the species studied here the cells of endodermis and pericycle that are located immediately adjacent to the protoxylem poles, did not show any cell wall thickening, unlike those adjacent to the phloem strands. However, the unthickened cell walls of the endodermis possess well-developed Casparian strips, so that the passage of water and solutes will be channeled primarily through the endodermis symplasm. According to Peterson and Enstone (1996), endodermal cells that contain only Casparian strips (stage I) are radially aligned with the protoxylem poles, and cell maturation in stages II (deposition of a suberin lamella) and III (addition of a lignified and cellulosic wall) is generally asynchronous, occurring first in those cells arranged radially to the phloem. In all of the roots analyzed, with the exception of P. corcovadense, the endodermis reaches the differentiation stage III showing “O”-shaped thickenings. Enstone et al. (2003) state that development of stages II and III in the endodermis provides protection against environmental stressors, such as desiccation, and confers mechanical support

to the root. Sufficient mechanical and physiological robustness is given, therefore, for all types of the investigated Philodendron roots, albeit structurally different according to their respective function.

Acknowledgment The authors would like to thank Ricardo Sousa Couto, for assistance in collection, Elaine Santiago Brilhante de Albuquerque, for revising an earlier version of the manuscript, and Coordenadoria de Aperfeic¸oamento do Pessoal de Nível Superior (CAPES), for financial support.

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