See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/292186879

Variation in the tracheary elements in species of Coryphantha (Cacteae- Cactoideae) with contrasting morphology: the bottleneck model

Article in Brazilian Journal of Botany · January 2016 DOI: 10.1007/s40415-016-0249-z

CITATIONS READS 5 163

3 authors, including:

Teresa Terrazas Monserrat Vázquez-Sánchez Universidad Nacional Autónoma de México Colegio de Postgraduados

309 PUBLICATIONS 3,735 CITATIONS 25 PUBLICATIONS 241 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Sistemática de Leiboldiinae (Vernonieae, Asteraceae) View project

Pit membrane of selaginella View project

All content following this page was uploaded by Monserrat Vázquez-Sánchez on 02 February 2016.

The user has requested enhancement of the downloaded file. Variation in the tracheary elements in species of Coryphantha (Cacteae- Cactoideae) with contrasting morphology: the bottleneck model

Teresa Terrazas, Rocío Escamilla-Molina & Monserrat Vázquez-Sánchez

Brazilian Journal of Botany

ISSN 0100-8404

Braz. J. Bot DOI 10.1007/s40415-016-0249-z

1 23 Your article is protected by copyright and all rights are held exclusively by Botanical Society of Sao Paulo. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.

1 23 Author's personal copy

Braz. J. Bot DOI 10.1007/s40415-016-0249-z

Variation in the tracheary elements in species of Coryphantha (Cacteae-Cactoideae) with contrasting morphology: the bottleneck model

1 1 2 Teresa Terrazas • Rocı´o Escamilla-Molina • Monserrat Va´zquez-Sa´nchez

Received: 21 September 2015 / Accepted: 13 January 2016 Ó Botanical Society of Sao Paulo 2016

Abstract A comparative analysis was conducted of the in the tubercles were two- or threefold wider than those of tracheary elements of the stem and tubercle of six species the vessel elements in the cortical vascular bundles. of Coryphantha. The aims of the study were to identify the Therefore, the results for the species of Coryphantha are micromorphological characters and to determine whether consistent with the bottleneck model observed for the the bottleneck model applied based on the similarity of the diameters of vessel elements for the non-succulent stems of diameters of the tracheary elements in the stem and in the other eudicots. tubercle. We collected individuals of C. bumamma, C. clavata, C. erecta, C. glanduligera, C. ottonis, and C. Keywords Cactaceae Á Helical secondary walls Á radians, which were species with contrasting morphologies Secondary growth Á Vessel elements Á Wide-band tracheids of the stems and tubercles. Sections and macerations were used to prepare the vascular cylinder and the cortical vas- cular bundles of the tubercle for observation. Our results Introduction showed that wide-band tracheids and vessel elements with annular or helical secondary walls predominated in wood. The genus Coryphantha is in the tribe Cacteae of the The cortical vascular bundles had primary or both primary subfamily Cactoideae in the Cactaceae. Species of Co- and secondary growths, and the tracheary elements had ryphantha have globose, depressed-globose, and cylindri- diameters of 10–27 lm, with the pattern and size of the cal stems (Bravo-Hollis and Sanche´z-Mejorada 1991; wide-band tracheids more heterogeneous than those of Va´zquez-Sa´nchez et al. 2012) with tubercles of different wood. These wider and shorter wide-band tracheids are sizes and forms that are rounded, ovoid, or conical and interpreted as analogous to the dilated tracheids in the have a base which is round, square, or rhomboid in shape, veinlets of eudicotyledons. The length and diameter of both with height varying from 8 to 12 mm. The wood anatomy tracheary elements (vessel elements and wide-band tra- of the five species of Coryphantha is similar to that of the cheids) in the tubercles were shorter and narrower than other members of Cacteae (Gibson 1973; Mauseth et al. those of the tracheary elements in the vascular cylinder of 1995;Va´zquez-Sa´nchez and Terrazas 2011), and the wood the stem (P \ 0.05). The diameters of the vessel elements has solitary vessels, abundant wide-band tracheids (WBT), and rarely, fibers. In the other members of Cactoideae, other features are observed in the wood, which include vessel elements with simple perforation plates, septate or & Teresa Terrazas non-septate libriform fibers, scarce paratracheal par- [email protected] enchyma, and the occurrence of stratified elements (Mau- seth and Plemons-Rodriguez 1998). The different cell types 1 Instituto de Biologı´a, Universidad Nacional Auto´noma de Me´xico, Ciudad Universitaria, 04510 Mexico City, Mexico found in the wood of Cactoideae, as in other eudicots, are essential for water movement, mechanical support, and 2 Centro Interdisciplinario de Investigacio´n para el Desarrollo Integral Regional, Unidad Michoaca´n, Jiquilpan de Jua´rez, storage of reserves, which are all required for plant survival 59510 Michoaca´n, Mexico (Va´zquez-Sa´nchez and Terrazas 2011). For example, in 123 Author's personal copy

T. Terrazas et al.

Cactoideae, fibers help in retaining the living protoplast by diameter and length of tracheary elements of the tubercles providing support and also in storing starch (Gibson 1973; are not available; however, recent studies suggest that the Va´zquez-Sa´nchez and Terrazas 2011), and successful wood of early derived Cacteae has narrow tracheary ele- conduction depends on the number, diameter, and perme- ments in species with different shapes and sizes (Va´zquez- ability of the tracheary elements (Mauseth and Plemons- Sa´nchez and Terrazas 2011). The genus Coryphantha was Rodriguez 1998). selected as the study system because of the wide diversity The leaves in Cactoideae are greatly modified, and the in the form and size of tubercles in different species, as primary photosynthetic organ is the stem (Mauseth 2006). noted previously, and this variability accounts for much of Morphologically, the tubercles in Cactoideae correspond to the diversity of these tubercles within the tuberculate stems a hypertrophied leaf base (Boke 1944; Bravo-Hollis 1978), of the Cacteae. We hypothesized that the bottleneck model and the size and form are important criteria for differen- would apply to the tracheary elements of Coryphantha tiating species (Bravo-Hollis 1978; Dicht and Lu¨thy 2003). tubercles as in other leafy eudicots. The aims of this study The distal part of the areole contains the tectriz leaf, and were to describe and compare the characteristics of the the proximal part contains several lateral meristems and secondary xylem of the stem and the xylem in the cortical produces a number of modified leaves (i.e., spines or bundles of the tubercles in six species of Coryphantha with bristles). The non-photosynthetic leaves are extremely contrasting morphologies and to evaluate whether the small and have little or no vascular tissue, and therefore bottleneck model applied to the genus. photosynthesis occurs in the tuberculate or ribbed stem (Mauseth 2006). Sajeva and Mauseth (1991) and Mauseth (2006) noted that the vascular cylinder of the photosyn- Materials and methods thetic stem connects to the stomata, which occur through- out the stem, through cortical bundles or foliar traces that Seventeen healthy, mature plants of six species of Co- are analogous to the veins in leafy eudicots. ryphantha were collected for the study (Table 1). The In other eudicots, a positive allometric relationship is plants were all collected during the rainy season from observed between leaf size and vascular properties (e.g., natural populations. The height and diameter of each plant vessel diameter in petioles) (Coomes et al. 2008), which were recorded. The spines were removed, and the stems demonstrates the principle that large leaves require an were divided into three sections: basal, middle, and apical extensive conductive system (tracheary elements) to pro- (Fig. 1a). The vascular tissue of the basal stem and of the vide a greater transpiration surface that contributes to cortical bundles of the tubercle was prepared for sections increased hydraulic resistance at the apex (Sack and Hol- (transverse and longitudinal) and macerations (Fig. 1b, c). brook 2006). The hydraulic resistance of the leaves (Rl)isa The segments were fixed in formalin–acetic acid–alcohol bottleneck model (pipe model), which is related to the (FAA, Ruzin 1999) for 48 h and then were washed with structure of the leaf that limits gas exchange and causes running water and stored in a solution of ethyl alcohol, physical damage to the major veins (Sack et al. 2004). water, and glycerin (GAA, 1:1:1) until sectioning. The Zimmermann (1983) notes that the bottleneck model can samples were paraffin-embedded following the technique be applied to all appendices of the stem, including bran- of Loza-Cornejo and Terrazas (1996) and were sectioned to ches, leaves, and inflorescences, because the diameters of a thickness of 12–15 lm with a rotary microtome. The the tracheary elements are narrower primarily at the sections were stained with safranin-fast green and mounted insertions of these appendices. In the Cactoideae with in a synthetic resin. significant reduced leaves, the assumption is that the bot- tleneck model applies between the green stems and the Wood and tubercle bundle maceration cortical bundles (xylem) of the tubercles, which are inter- preted as analogous to leaf veins (Mauseth and Sajeva For the macerations of the vascular cylinder, one or more 1992). However, it is unknown whether the bottleneck fascicules of 5 mm long were separated and only the first model applied to Cactoideae because the tracheary ele- 2 mm near the vascular cambium was used. For the mac- ments of the tubercles and those of the stems have not been erations of the tubercle, we removed all parenchyma from compared. Although Mauseth and Sajeva (1992) found that the epidermis to the inner cortex using a stereomicroscope, the tracheary elements in the cortical bundles are narrower in addition to the parenchyma surrounding the cortical (3.6–14.6 lm) than those of the vascular cylinder bundles. For both the cylinder and the tubercle, the vas- (46–56 lm) in the ribbed stem of Subpilocereus repandus cular tissue was macerated with the addition of 2 ml of (L.) Backeb.; this difference in morphology of the width of Jeffrey solution (Johansen 1940) per tube. To accelerate the the tracheary elements was not related to the bottleneck or cellular separation process, the tubes were placed in an pipe model. For most Cacteae members, information on the oven at 50 °C for 1 h for the vascular cylinder xylem and 123 Author's personal copy

Variation in the tracheary elements in species of Coryphantha (Cacteae-Cactoideae)…

Table 1 Growth forms, tubercles, and sizes of plants per species collected Species Growth forms and tubercles State Size (length 9 diameter, cm) Collector

C. bumamma (Ehrenberg) Globose-depressed, tubercles large, Oaxaca A.17.0 9 10.2 TT801 Britton & Rose conical, rounded, upper part flattened, at B.16.0 9 9.8 base 27 mm wide C. ottonis (Pfeiffer) Lemaire Globose, tubercles large, rounded, broad State of Mexico A.12.0 9 8.2 TT931 conical, at base 18 mm wide B.11.5 9 8.8 C. radians (A.P. de Candolle) Globose, tubercles ovoid, rhomboid at San Luis Potosı´ A.6.3 9 4.4 TT877, Britton & Rose base, at base 12–16 mm wide B.4.2 9 5.3 A.11.0 9 8.6 SA1700 B.9.7 9 8.9 C. glanduligera Lemaire Globose, conical slightly concave, with 4 San Luis Potosı´ A.13.1 9 5.2 TT824, edges at the base, at the base 14 mm B.15.0 9 4.8 wide A.15.0 9 5.0 TT834 B.18.0 9 6.6 C. clavata (Scheidweiler) Cylindric, tubercles conical, rounded, Hidalgo A.11.0 9 9.7 TT963, Backeberg flattened on top B.10.0 9 8.8 36.0 9 12.1 SA1705 C. erecta (Lemaire ex Pfeiffer) Cylindric, tubercles oblique, conical, Quere´taro 28.0 9 7.9 SA1672, Lemaire flattened on top at base rhomboid, at 38.0 9 6.9 SA1684 base 10 mm wide In some localities, the same collector number was assigned to two plants (letters A and B). All herbarium vouchers at MEXU

Fig. 1 Sectioning for anatomical study. a Coryphantha clavata without spines and stems divided into three regions. b, c Diagrams showing sampling for the stem and for the tubercle vascular tissue. ca closed to the areole, fa far from the areole

for 3 to 4 h for the tubercles. Additionally, the tubes were Quantification and observation vibrated in a sonicator until cell separation and then rinsed with water to remove the Jeffrey solution. The macerations The length and diameter of 50 cells per tracheary element were stained with 1 % aqueous toluidine and mounted with (vessel elements and WBTs) and the fibers were measured gelatin glycerin. All the measurements were performed on in the macerations. Additionally, to evaluate diversity of temporary slides. tracheary elements based on position within the tubercle,

123 Author's personal copy

T. Terrazas et al. the diameters of 25 tracheary elements were measured in and the sections and macerations were both photographed the transverse sections of the cortical bundles. The mea- to illustrate the variation in the tracheary elements. surements were performed with an image analyzer (Image- Pro PlusÒ6.1, Media Cybernetics, Silver Spring, MD, USA) adapted for a compound microscope. To evaluate the Results differences in the tracheary elements between the tubercle and the vascular cylinder, an analysis of variance was In the stem secondary xylem, the vessels were embedded in performed using the SAS statistical software package (SAS a WBT matrix with scanty paratracheal parenchyma and 2008). Both the transverse and longitudinal sections were non-lignified rays (Figs. 2–9). Furthermore, in three spe- used to describe the characteristics of the vascular tissue, cies, the axial parenchyma was distributed in tangential

Figs. 2–9 Coryphantha wood: 2–5 Transverse sections: 2 C. erecta, highly homogeneous wood. 3 C. glanduligera, tangential bands of parenchyma. 4 C. radians, details of wide-band tracheids. 5 C. glanduligera, details of vessels embedded in a band of parenchyma and a few wide-band tracheids. 6–9 Tangential sections: 6 C. erecta, simple perforation plate in a vessel element. 7 C. bumamma, stratified tracheary elements. 8 C. glanduligera, multiseriate non-lignified rays. 9 C. ottonis, fibers. Bar is 300 lmin2, 3, 8; 100 lmin4, 5, 7, 9,20lmin6

123 Author's personal copy

Variation in the tracheary elements in species of Coryphantha (Cacteae-Cactoideae)…

Figs. 10–27 Tracheary elements in Coryphantha: 10–13 Vessel elements in wood: 10 C. bumamma. 11 C. erecta. 12 C. radians. 13 C. clavata. 14–17. WBT in wood: 14 C. bumamma. 15 C. erecta. 16 C. ottonis 17 C. radians. 18–22 Vessel elements in cortical bundles. 18 C. radians. 19 C. bumamma. 20 C. glanduligera. 21 C. ottonis. 22 C. ottonis. 23–27 WBT in cortical bundles: 23 C. ottonis. 24 C. glanduligera. 25 C. clavata. 26 C. ottonis. 27. C. glanduligera. Bar is 50 lm bands in which vessels were embedded that alternated with For the patterns of accumulation of the secondary walls the WBT matrix (Figs. 3, 5). The WBTs and vessels in and the lengths, the morphological diversity of the trac- transverse section were difficult to differentiate because heary elements was high (Figs. 10–27; Tables 2, 3). As both tracheary elements had similar wall thicknesses mentioned previously, in the vessel elements, the perfora- (Figs. 2, 4). In the tangential sections, the vessel elements tion plates were simple, with the secondary wall arranged had simple perforation plates, and both tracheary elements in an annular, open, or closed helical pattern (Figs. 10–13). had annular and helical secondary walls that might have a The vessel elements were relatively short, and their mean weak stratified pattern (Figs. 6–8). The rays were hetero- values of length ranged from 124.67 lminC. erecta to geneous and multiseriate with 2- to 5-seriate thin, non- 187.66 lminC. bumamma; their diameters ranged from lignified primary walls (Fig. 8), and the fibers were libri- 25.03 lminC. erecta to 39.33 lminC. bumamma form, non-septate, rare, and only observed in some tan- (Table 2). For the WBTs, the secondary wall was primarily gential sections (Fig. 9). helical, with additional annular thickening that occurred in

123 Author's personal copy

T. Terrazas et al.

Table 2 Diameter and length Cylinder Tubercle of vessel elements (mean ± standard error) in the Diameter Length Diameter Length vascular cylinder and tubercles of Coryphantha species C. bumamma 39.33 ± 3.00A 187.66 ± 952a 15.00 ± 1.41B 209.66 ± 49.9a quantified in macerations C. ottonis 37.51 ± 5.12A 129.17 ± 18.08a 21.23 ± 8.27B 157.80 ± 24.80a C. radians 34.40 ± 6.63A 164.59 ± 7.37a 15.83 ± 1.47B 164.36 ± 8.12a C. glanduligera 33.50 ± 1.04A 133.01 ± 17.12a 11.00 ± 0.89B 180.50 ± 12.51b C. clavata 31.5 ± 1.04A 128.50 ± 6.09a 10.08 ± 1.28B 137.001 ± 15.70a C. erecta 25.00 ± 1.00A 124.66 ± 3.06a 10.00 ± 1.00B 123.35 ± 5.03a Letters indicate statistical differences (P = 0.05, Tukey); capital letters for diameter in rows and lower case letters for length

C. bumamma and C. glanduligera (Figs. 14–17), whereas two- or threefold wider in the vascular cylinder (Table 2). the length varied from 117.00 lminC. ottonis to For the diameters of the WBTs, differences were also 178.33 lminC. bumamma; the diameters ranged from detected (F [ 238.91, P \ 0.0001; Table 3); however, the 31.10 lminC. erecta to 49.03 lminC. bumamma diameters were only one- or twofold wider in the vascular (Table 3). cylinder than those in the tubercle. The lengths of the In the tubercles, the vascular tissue was in the collateral tracheary elements were also different between the vascu- cortical bundles which were scattered subjacent to the lar cylinder and the tubercle, but only for a few species palisade parenchyma and near the areola. These cortical with C. glanduligera for the vessel elements (F = 80.48, bundles had primary or both primary and secondary P \ 0.0001; Table 3) and C. bumamma and C. clavata for growths (Figs. 28–36). In the cortical bundles, substantial the WBTs (F [ 84.73, P \ 0.0001; Table 3). diversity was observed for the diameters of the tracheary elements. For example, in C. erecta, the diameter was relatively constant throughout the bundle (Fig. 28), Discussion whereas in other species, the diameters were narrower in the center of the bundle and larger toward the periphery Characterization of tracheary elements (Figs. 29–34). Additionally, in C. ottonis, the larger trac- heary elements were distributed on one side of the bundle The wood of the six species of Coryphantha was similar to only (Fig. 31) or were all around the xylem (Fig. 29). the general pattern reported for other members of Cacteae Typically, compared with those found in the periphery of (Mauseth and Plemons-Rodriguez 1998;Va´zquez-Sa´nchez the tubercle, the tracheary elements of the cortical bundles and Terrazas 2011; Grego-Valencia et al. 2015), although near the areola had diameters that were narrower (Table 4). differences were found for the size of tracheary elements of In the macerations of the cortical bundles, the vessel some species that were related to the size of the species, as elements and their morphologies were clearly identified to reported for other members of this tribe (Va´zquez-Sa´nchez be different from the WBTs (Figs. 18–27). In C. erecta, the and Terrazas 2011). Similar to the species of Coryphantha cells were difficult to separate because the tracheary ele- examined in the study, in other species of this tribe, WBTs ments were compact and had narrow diameters (Fig. 28). are the most abundant cell type in a matrix in which vessels Similar to the tracheary elements of the vascular cylinder, and scanty paratracheal parenchyma are embedded with these vessel elements had simple perforation plates and non-lignified multiseriate rays. Additionally, in the sec- secondary walls with helical thickening exclusively, and ondary xylems of C. bumamma, C. glanduligera, and C. notable for both, the cells were shorter and wider (Figs. 22, radians, the vessels are located in regions with a matrix of 26, 27). The length of the vessel elements ranged from only parenchyma. According to Mauseth (1993) and 123.35 lminC. erecta to 209.66 lminC. bumamma, and Mauseth et al. (1995), earlywood is typified by the their diameters varied from 10.00 to 21.23 lm (Table 2). arrangement with embedded vessels in parenchyma, The WBTs also had secondary walls arranged with helical whereas the areas with WBTs characterize latewood. To thickening in the cortical bundles (Figs. 10–27), with mean confirm this hypothesis for the Coryphantha group of lengths ranging from 98.50 to 186.00 lm and mean species, vascular cambium studies are required. diameters ranging from 14.66 to 27.00 lm (Table 3). Fibers were found for C. erecta, C. ottonis, and C. For the diameters of the vessel elements, differences radians primarily only in the macerations. The fibers were were detected between the vascular cylinder and the not observed in cross sections but were observed in tan- tubercle (F [ 173.70, P \ 0.0001), with the diameters gential sections in the interfascicular region, as reported by

123 Author's personal copy

Variation in the tracheary elements in species of Coryphantha (Cacteae-Cactoideae)…

Table 3 Diameter and length Species Cylinder Tubercle of wide-band tracheids (mean ± standard error) in the Diameter Length Diameter Length vascular cylinder and tubercles of Coryphantha species C. bumamma 49.03 ± 3.00A 178.32 ± 14.23a 24.00 ± 5.21B 98.50 ± 11.32b quantified in macerations C. ottonis 41.00 ± 9.89A 117.00 ± 14.80a 24.80 ± 5.26B 137.40 ± 23.84a C. glanduligera 39.50 ± 3.93A 147.50 ± 41.46a 27.00 ± 2.16B 138.50 ± 18.61a C. clavata 32.51 ± 7.18A 125.50 ± 4.04a 15.50 ± 1.22B 186.00 ± 13.11b C. radians 32.50 ± 6.63A 174.00 ± 7.41a 16.41 ± 1.83B 170.50 ± 6.74a C. erecta 31.00 ± 1.00A 155.83 ± 5.47a 14.66 ± 2.52B 153.33 ± 2.88a Letters indicate statistical differences (P = 0.05, Tukey); capital letters for diameter in rows and lower case letters for length

Figs. 28–36 Coryphantha cortical bundles in tubercles: 28–32 Cortical bundles with primary growth: 28 C. erecta, tracheary elements similar sizes. 29 C. glanduligera, wider tracheary elements in the bundle periphery. 30 C. glanduligera, wider tracheary element in the distal part of the bundle. 31 C. ottonis, wider tracheary element on a side of the bundle. 32 C. bumamma, longitudinal section showing shorter wider tracheary element. 33–36 Cortical bundles with primary and secondary growth. 33 C. radians, non-functional phloem, (arrow). 34 C. bumamma, vascular cambium (asterisk) and non-functional phloem (arrow). 35 C. erecta. 36 C. radians. Bar is 20 lm

123 Author's personal copy

T. Terrazas et al.

Table 4 Mean values of the tracheary elements’ diameter in relation spaced for contraction and expansion, as recently demon- to the position of the cortical bundle in the tubercle strated empirically in Ariocarpus fissuratus (Garrett et al. Tracheary element’s diameter (lm) 2010). The WBTs have been described for several genera of Cactoideae (Mauseth et al. 1995; Arruda and Melo-de- Far from the areole Near areola Pinna 2010), and because Coryphantha is a genus of the C. bumamma 7.96–14.92 8.13–18.35 tribe Cacteae that is one of the earliest diversified in the C. ottonis 7.63–15.06 8.24–13.92 Cactoideae, the WBTs of the genus are likely ancestral C. radians 9.82–39.62 8.72–21.49 (Va´zquez-Sa´nchez et al. 2013). C. glanduligera 15.09–26.11 11.52–24.93 For the tubercles, most collateral cortical bundles C. clavata 4.97–12.87 6.65–11.60 developed secondary growth, and the secondary xylem and C. erecta 8.91–9.11 8.02–9.15 phloem produced by the vascular cambium in these tubercles are also recorded in other Cactoideae (Sajeva and Mauseth 1991; Mauseth and Sajeva 1992; Terrazas and Reyes-Rivera (2010) for C. clavata and for C. ottonis in Mauseth 2002; Mauseth 2006). The vessel elements have this study. The fibers did not increase in number as the simple perforation plates and lateral walls with helical secondary xylem accumulated, and therefore, the thickenings. No WBTs were found in the cortical bundles mechanical properties supporting the stem were not a result of six species of Cactoideae in the tribes Cereeae and of the fibers. The wood of Coryphantha was not rigid, Trichocereeae (Arruda and Melo-de-Pinna 2010); however, which is a property related to the globose or short, cylin- in this study, WBTs were observed in the cortical bundles drical stems of the species that may be advantageous in two of all species of Coryphantha (Fig. 3). The WBTs in the ways: (1) high energy cost to produce abundant secondary tubercles had dimensions that were more heterogeneous walls with lignin can be avoided, which contributes to than those of the vessel elements of the identical tubercles water economy (Nobel 1981) and (2) the stems can shrink (Table 3). Although several studies on Cactoideae describe during hydric stress and then expand significantly after cortical bundles and discuss their importance in under- rainfall, as reported for C. vivipara that survived 91 % standing the water economy of succulent stems, the water loss (Nobel 1981; Mauseth 1993). dimensions of tracheary elements have not been reported, The vessel elements had simple perforation plates and except for Subpilocereus repandus. generally, a helical pattern, with the exception of the annular pattern in C. erecta. The annular and helical Cortical bundles of the tubercle versus the vascular thickenings of the walls of vessel elements express xero- cylinder morphic features that operate at high water tensions (Carlquist 1977), with the helical forms of the bands The diameters of both tracheary elements were up to physiologically related to hydric stress. Additionally, the threefold narrower in the tubercle than the diameters of increase in the area of the walls might increase adherence those in the vascular cylinder; this reduction in the diam- to the surface of the walls to prevent embolism (Carlquist eters of the tracheary elements is interpreted as the ‘‘bot- 1988). This type of thickening can increase the wall tleneck,’’ which is found in the petioles of eudicot species strength of the vessel elements without an excessive with leaves or branches (Zimmermann 1983). Coomes increase in the flow resistance as noted by Zimmerman et al. (2008) noted that leaf area is related to the diameters (1983). of the tracheary elements of petioles because of the bot- The walls of the WBTs had annular, helical, and double- tleneck effect. Thus, the vessel elements are rearranged in helix thickenings, and these characteristics of the Co- secondary and tertiary veins so that as water passes from ryphantha species in this study also occur in other species the major veins to the minor ones a bottleneck is created as in North America, primarily in those of the tribe Cacteae the elements pass from the vascular bundles to the leaf (Gibson 1973; Mauseth 1993; Mauseth et al. 1995). petiole in eudicots (Sack and Holbrook 2006). Consistent According to Landrum (2006), the double-helix arrange- with the bottleneck model, in the analysis of four species of ment in the WBTs of the stems of Anacampseros Portulaca, Hernandes-Lopes and Melo-de-Pinna (2008) (Anacampserotaceae) provides structural reinforcement to found that the vessel diameters in leaves are twofold nar- prevent the collapse of primary wall cells; the interpreta- rower than those of the stem. Similarly, in the Coryphantha tion for Coryphantha species is that the WBTs with this species that were succulent and leafless, the diameters of arrangement may also function as the primary support in the vessels of the vascular cylinder of the stems were two- the absence of fibers. Furthermore, according to Mauseth or threefold wider than those in the tubercles. Additionally, et al. (1995), the thickening of the secondary wall of the form and shape of the tubercle did not affect the water annular or helical WBTs in the wood of cacti is widely movement. Therefore, the results for the Coryphantha 123 Author's personal copy

Variation in the tracheary elements in species of Coryphantha (Cacteae-Cactoideae)… species were consistent with the demonstrations of a bot- that have a mean of 14.47 lm and twice that diameter for tleneck discussed by Zimmermann (1983) and Coomes the WBTs in their stems (Landrum 2006); thus, for the et al. (2008). Most likely in these species, a bottleneck genera in these families, the comparison confirms that the favors the conduction of water in the tuberculate stems of diameters of the WBTs and the vessel elements are con- these species, particularly during the flowering stage when sistent with the bottleneck model. The heterogeneity of the there is an increased demand for water. A bottleneck was tracheary elements of the tubercle in the species of Co- also confirmed for Subpilocereus repandus, a species with ryphantha examined in this study might be because they ribbed stems in which the cortical bundles have vessel were derived from elements of the procambium and the diameters (3.6–14.6 lm) that are narrower than those of vascular cambium. the stem (46–56 lm) (Mauseth and Sajeva 1992), based on our results. Moreover, these results suggest that this trait is Acknowledgments The financial support for this research is highly conserved in cacti, despite the impressive morpho- appreciated and was provided through a grant from the Programa de Apoyo a Proyectos de Investigacio´n de Innovacio´n Tecnolo´gica, logical diversity and the reduction of plant organs DGAPA, Universidad Nacional Auto´noma de Me´xico (IN209012, responsible for photosynthesis. Based on the bottleneck IN210115) to TT. Thanks to Salvador Arias for helping in the field model in this study, our results support the ’ power scaling work. Art work by Julio Ce´sar Montero Rojas and Diana Martı´nez is of the photosynthetic surface area in plants, which is also appreciated. We appreciate the comments of the reviewers that allow us to clarify some ideas. apparently universal in gymnosperms and angiosperms (Price and Enquist 2006). In future research, whether the identical morphology occurs in the vascular cylinders of References species with a greater proportion of succulence, e.g., Echinocactus and Ferocactus, should be determined, as Arruda E, Melo-de-Pinna GF (2010) Wide-band tracheids (WBTs) of noted by Va´zquez-Sa´nchez and Terrazas (2011). photosynthetic and non-photosynthetic stems in species of For the WBTs, the diameters were twofold wider in the Cactaceae. J Torrey Bot Soc 137:16–29 Boke NH (1944) Histogenesis of the leaf and areole in Opuntia vascular cylinder than those in the tubercle. Based on the cylindrica. Am J Bot 31:299–316 variability observed in the cortical bundles, the WBTs Bravo-Hollis H (1978) Las cacta´ceas de Me´xico, vol I. Universidad tended to be more heterogeneous in size (Figs. 3, 4); this Nacional Auto´noma de Me´xico, Me´xico ´ ´ variation most likely favored horizontal water flow com- Bravo-Hollis H, Sanchez-Mejorada H (1991) Las cactaceas de Me´xico, vol II. Universidad Nacional Auto´noma de Me´xico, pared with vertical flow. Moreover, in three of the species Me´xico studied, one or more shorter and wider WBTs occurred in Carlquist S (1977) Ecological factors in wood evolution: a floristic the margin of the cortical vascular bundle in the tubercle. approach. Am J Bot 64:887–896 Carlquist S (1988) Comparative wood anatomy: systematic, ecolog- These WBTs are apparently analogous to the dilated tra- ical and evolutionary aspects of dicotyledon wood. Springer- cheids described in the veinlets of several eudicot leaves Verlag, Berlin (Tucker 1964; Rao and Das 1979; Lersten and Curtis 1996; Coomes D, Heathcote S, Godfrey E, Shepherd J, Sack L (2008) Luckow 2002; Hernandes-Lopes and Melo-de-Pinna 2008) Scaling of xylem vessels and veins within the leaves of oak and therefore are likely reservoirs of water. However, species. Biol Lett 4:302–306 Dicht R, Lu¨thy A (2003) Coryphantha: cacti of Me´xico and southern ontogenetic studies are needed to understand their origin. If USA. Springer-Verlag, Berlin these WBTs store water as proposed, they will have a Garrett TY, Huynh CV, North GB (2010) Root contraction helps function similar to that described for the 3D-venation of protect the ‘‘living rock’’ cactus Ariocarpus fissuratus from succulent-leaved Portulacineae (Ogburn and Edwards lethal high temperatures when growing in rocky soil. Am J Bot 97:1951–1960. doi:10.3732/ajb.1000286 2013). In succulent stems, the external layers of photo- Gibson A (1973) Comparative anatomy of secondary xylem in synthetic cells and internal water storage tissues are spa- Cactoideae (Cactaceae). Biotropica 5:29–65 tially separated. The movement of water from the Grego-Valencia D, Terrazas T, Lara-Martı´nez R, Jime´nez-Garcı´aLF (2015) La membrana de la punteadura en dos especies de Cacteae, chlorenchyma to the xylem and the internal redistribution Cactaceae. Bot Sci 93:209–219. doi:10.17129/botsci.145 of water among stem tissues are dominated by changes in Hernandes-Lopes J, Melo-de-Pinna GF (2008) Ana´lise morfome´trica the osmotic pressure of the chlorenchyma (Schulte et al. dos elementos traqueais em quatro espe´cies de Portulaca 1989). Thus, the vessel elements and WBTs in the cortical (Portulacaceae). Acta Bot Bras 22:607–613 bundle contribute to water movement and storage. More- Johansen DA (1940) Plant microtechnique. Mc.Graw-Hill, New York Landrum JV (2006) Wide-band tracheids in genera of Portulacaceae: over, as demonstrated by Reyes-Rivera et al. (2015), the novel, non-xylary tracheids possibly evolved as an adaptation to rigidity of the secondary walls of these cells helps maintain water stress. J Plant Res 119:497–504. doi:10.1007/s10265-006- the continuity of conductivity by providing protection for 0013-8 the vessels when turgor is lost. The WBTs in Coryphantha Lersten NR, Curtis JD (1996) Survey of leaf anatomy, especially secretory structures, of tribe Caesalpinioideae (Leguminosae, had similar diameters to those recorded in the leaves of Caesalpinioideae). Plant Syst Evol 22:189–198. doi:10.1007/ Portulacaceae and Ruschioideae (Aizoaceae), with genera BF00984746 123 Author's personal copy

T. Terrazas et al.

Loza-Cornejo S, Terrazas T (1996) Anatomı´a del tallo y de la raı´zde relationship between lignification and stem morphology. PloS dos especies de Wilcoxia Britton y Rose (Cactaceae) del noreste One PONE-D-14-38958R1. doi: 10.1371/journal.pone.0123919 de Me´xico. Bol Soc Bot Me´x 59:13–23 Ruzin SE (1999) Plant microtechnique and microscopy. Oxford Luckow M (2002) Anatomical features of the leaves in the University Press, New York Dichrostachys group (Leguminosae: Mimosoideae) and their Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol utility for phylogenetic studies. Syst Bot 27:29–40 57:361–381 Mauseth JD (1993) Water-storing and cavitation-preventing adapta- Sack L, Streeter C, Holbrook NM (2004) Hydraulic analysis of water tions in wood of cacti. Ann Bot-London 72:81–89. doi:10.1006/ flow through leaves of sugar maple and red oak. Plant Physiol anbo.1993.1083 134:1824–1833. doi:10.1104/pp.103.031203 Mauseth JD (2006) Structure-function relationships in highly mod- Sajeva M, Mauseth JD (1991) Leaf-like structure in the photosyn- ified shoots of Cactaceae. Ann Bot-London 98:901–926. doi:10. thetic, succulent stems of cacti. Ann Bot-London 68:405–411 1093/aob/mcl133 SAS Institute (2008) SASÒ 9.1 users guide statistics. SAS Institute Mauseth JD, Plemons-Rodriguez B (1998) Evolution of extreme Inc., Cary xeromorphic characters in wood: a study of nine evolutionary Schulte PJ, Smith JAC, Nobel PS (1989) Water storage and osmotic lines y Cactaceae. Am J Bot 85:209–218 pressure influences on the water relations of a dicotyledonous Mauseth JD, Sajeva M (1992) Cortical bundles in the persistent desert succulent. Plant Cell Environ 12:831–842. doi:10.1111/j. photosynthetic stems of cacti. Ann Bot-London 70:317–324 1365-3040.1989.tb01646.x Mauseth JD, Uozumi Y, Plemons B, Landrum J (1995) Structural and Terrazas T, Mauseth J (2002) Shoot anatomy and morphology. In: systematic study of an unusual tracheid type in cacti. J Plant Res Nobel P (ed) Cacti biology and uses. University of California 108:517–526. doi:10.1007/BF02344242 Press, Berkeley, pp 23–40 Nobel PS (1981) Influence of freezing temperatures on a cactus, Tucker SC (1964) The terminal idioblasts in Magnoliaceous leaves. Coryphantha vivipara. Oecologia 48:191–198 Am J Bot 51:1051–1062 Ogburn RM, Edwards EJ (2013) Repeated origin of three-dimensional Va´zquez-Sa´nchez M, Terrazas T (2011) Stem and wood allometric leaf venation releases constraints on the evolution of succulence relationships in Cacteae (Cactaceae). Trees-Struct Funct in plants. Curr Biol 23:722–726. doi:10.1016/j.cub.2013.03.029 25:755–767. doi:10.1007/s00468-011-0553-y Price CA, Enquist BJ (2006) Scaling of mass and morphology in Va´zquez-Sa´nchez M, Terrazas T, Arias S (2012) El ha´bito y forma de plants with minimal branching: an extension of the WBE model. crecimiento en la tribu Cacteae (Cactaceae, Cactoideae). Bot Sci Funct Ecol 20:11–20. doi:10.1111/j.1365-2435.2006.01078.x 90:97–108 Rao TA, Das S (1979) Typology of foliar tracheoids in angiosperms. Va´zquez-Sa´nchez M, Terrazas T, Arias S, Ochoterena H (2013) Proc Indian Acad Sci 88:331–345 Molecular phylogeny, origin, and taxonomic implications of Reyes-Rivera J (2010) Ontogenia de la madera en tallos contrastantes tribe Cacteae (Cactaceae). Syst Biodivers 11:103–116. doi:10. de la tribu Cacteae. Tesis de Maestrı´a Posgrado en Ciencias 1080/14772000.2013.775191 Biolo´gicas. Instituto de Biologı´a, Universidad Nacional Auto´n- Zimmermann MH (1983) Xylem structure and the ascent of sap. oma de Me´xico, Mexico Springer-Verlag, Berlin Reyes-Rivera J, Canche´-Escamilla G, Soto-Herna´ndez M, Terrazas T (2015) Wood chemical composition in species of Cactaceae: The

123

View publication stats