Comparative Anatomical Analysis of three Rumex L. Species (Polygonaceae): Stem and Leaf Cross-sections Study

 

Rand AlKhoury*, Racha AlKhatib

Department of Pharmacognosy, Faculty of Pharmacy, Damascus University, Damascus, Syria.

 

ABSTRACT:

Rumex species (Polygonaceae) have very similar morphological characteristics and are challenging to classify depending on the shape of fruits as a taxonomic key. Previous studies have proven the importance of anatomical and microscopic characteristics in finding diagnostic elements for identifying plant species. To our knowledge, there is a lack of studies on the leaf and stem anatomy of Rumex L. species. Therefore, this research aims to investigate the anatomical features of stem and leaf cross-sections of Rumex conglomeratus, Rumex chalepensis and Rumex pulcher grown wild in Syria. Fresh plants were collected from various regions during fructification stage. Fresh young parts of stems and leaves were taken and cross-sections were made manually and stained using iodine green - carmine double coloration. The colored cross-sections were examined using a light microscope. This research represents the first detailed anatomical study of leaf cross-sections in three species of Rumex L. grown wild in Syria. The results highlighted 12 qualitative and 10 quantitative features of stem and leaf cross-sections. Only the stem of R. conglomeratus contained calcium oxalate crystals. Papillary trichomes were only present on the leaves of R. pulcher. The shape of stem and leaf cross-sections, the number of vascular bundles in leaf cross-sections, vascular bundle’s diameter, parenchyma layers and thickness, and the number of collenchyma layers exhibited significant differences among the studied species and could be taxonomically important in their classification.

 

 

 

INTRODUCTION: 

The Polygonaceae family is widely distributed in most parts of the world. It includes nearly 50 genera and 1,200 species of flowering herbs, shrubs, or climbing plants ¹. The most important genera are Polygonum, Rumex, Rheum, Persicaria, and Coccoloba^1,2. The genus Rumex L. is the second-largest genus in the Polygonaceae family, with 200 species widely distributed worldwide, especially in the Northern temperate zone^3,4. Rumex plants are popularly used to treat many diseases such as infections⁵, skin diseases⁶, leishmania⁷, diarrhea ⁸, constipation ^9,10, jaundice¹, and cancer^11,4, and the roots have been widely used as laxatives^12,5.

 

These medicinal uses are related to the various content of secondary metabolites that possess many important biological activities¹³, such as polyphenols¹⁴, flavonoids, anthraquinones, tannins, stilbenes, terpenes, and many others^4,15.  In addition, the leaves of many species have a distinct acidic taste and are consumed as food in many regions^12,16.

 

Rumex species have very similar morphological characteristics and are challenging to classify¹⁵. In general, they are herbaceous plants with straight stem, usually branched. The leaves are alternate, the flowers are hermaphroditic or unisexual, and the perianth consists of 6 segments. The valves are triangular, oval, or cordate, and they may be membranous or leathery, with entire or dentate margins. The fruit is an achene, resembling a tubercle located in the midrib of the valves ^17,18. The classification of species relies on the shape of fruits as a taxonomic key^19,15.

 

 

Previous studies have proven the importance of anatomical and microscopic characteristics in finding diagnostic elements for identifying plant species and solving taxonomic issues^20,21. Many anatomical features greatly help in distinction between species²², whether the shape and arrangement of stem and leaf tissues, venation patterns, or the presence or absence of some anatomical structures, such as trichomes, stomata, or specialized tissues^23,24. Soleimani et al. studied the stem and leaf anatomy and pollen characters of five Rumex L. species in Iran, including R. conglomeratus and R. chalepensis. They discussed various features of the collenchyma and sclerenchyma tissues, vascular bundles, and pollens ²⁵.  Keshavarzi et al. studied the anatomy of the stem and identified various quantitative and qualitative anatomical features of six Rumex L. species in Iran. They reported the presence of collateral vascular bundles only in R. chalepensis and the absence of calcium oxalate crystals only in R. elbrusensis. They also found that the stomata type is anisocytic in all species studied, but the differences were in the size of epidermal and stomata cells¹⁹. Mohamed and Azer studied the morphological and anatomical features of eight Polygonaceae plants in Egypt, including R. vesicarius and R. dentatus²⁶.

 

In Syria, Rumex L. genus is represented by 12 species¹⁸, R. conglomeratus Murr., R. chalepensis Mill., and R. pulcher L. are among the most widespread species, and are traditionally used by local people to treat many illnesses, and are also consumed as food. These species are morphologically similar to a large extent, and it is difficult to distinguish between them. To our knowledge, there are no previous studies on the leaf anatomy of the three mentioned species, and the shape of the stem’s cross-section has not been determined yet. Therefore, this research aims to investigate 10 quantitative and 12 qualitative anatomical features of stem and leaf cross-sections made manually from three Rumex species grown in Syria; R. conglomeratus Murr., R. chalepensis Mill., and R. pulcher L. using a light microscope and proper statistical analysis tests, to compare and distinguish the most significant anatomical differences that can help in classifying these Rumex species.

 

MATERIALS AND METHODS:

Materials:

Plant material:

Fresh plants of R. conglomeratus, R. chalepensis and R. pulcher were collected from various regions of Syria in May – June 2023 during the fructification stage, three to four months after leafing (Figure 1). Species were identified by Dr. Ahmad Jadouaa, Faculty of Agriculture, Aleppo University, according to the new flora of Lebanon and Syria by Mouterde (1966). Taxa information (Location, Geographical Coordinates, Date of collection and Altitude) are mentioned in Table 1.

Table 1: Taxa information

Taxon name	Location and date of collection	Coordinates	Altitude
Rumex conglomeratus Murr.	Damascus countryside - Ain Mneen - 6/6/2023	33°38′32″N 36°17′52″E	1200 m
Rumex chalepensis Mill.	Damascus countryside - Ain Mneen - 9/5/2023	33°38′32″N 36°17′52″E	1200 m
Rumex pulcher L.	Tartus - Duwayr Taha - 11/5/2023	34°58′15″N, 35°55′0″E	22   m

 

Figure 1: Fresh plants of Rumex L. during the collection time: a; R. conglomeratus Murr., b; R. chalepensis Mill., c; R. pulcher L.

 

Methods:

Cross-sectioning and staining:

The cross-sections were made following the method of Soorya et al. with some modifications²⁷. Fresh parts of stems and leaves were taken to make cross-sections. The vegetative part was placed vertically on a slide. Thin and transparent cross-sections were manually made using a new sharp blade. The cross-sections were soaked in sodium hypochlorite for 20 minutes to break down the cellular content and preserve the cell walls. Then, they were washed twice and immersed in 20% acetic acid for 5 to 10 minutes. After that, they were stained with iodine green – red carmine double coloration (a mixture of iodine green and carmine alumina, purchased from Serva, Germany) for 10 minutes. The cellulose tissues were colored pinkish-red, and the lignified tissues were colored green. The colored sections were then placed on a slide with drops of glycerin and examined using the light microscope (Olympus Optical, Model CHT, Japan) at total magnifications of x100 and x400.

 

Statistical Analysis:

Anatomical structures of the stem and leaf were studied by 10 quantitative features which are: Vascular bundle’s diameter in stem and leaf, the number of vascular bundles in stem and leaf, parenchyma layers and thickness in groove’s zone in stem, collenchyma layers in stem and leaf, palisade and spongy parenchyma layers in leaf. And 12 qualitative features including the shape of stem cross-section, the arrangement of ribs and grooves, the shape of ribs, collenchyma type, and the presence/absence of cortical parenchyma, internal vascular bundles, calcium oxalate crystals in stem and leaf, hollow pith, palisade parenchyma, and trichomes.

 

Measurements were taken between 10 to 50 readings for each specimen. A descriptive statistical analysis was conducted (Mean, max, min, median, and mode were calculated for the quantitative features) using Microsoft Office Excel 2016 to enrich the results. The data obtained in this study were analyzed using both parametric and non-parametric statistical tests to ensure the robustness and reliability of the results using SPSS software version 25. The normality of the data was evaluated by calculating skewness and kurtosis. One-way ANOVA test was conducted to compare the means when the data met the assumptions of normality and homogeneity of variances. The Kruskal-Wallis test was also employed to compare groups when the assumptions of normality are violated. Post-hoc analysis was conducted to examine pairwise significance between each pair of species. Both the ANOVA and Kruskal-Wallis tests were performed at a significance level of p < 0.05.

 

RESULTS:

By using double staining, we were able to distinguish the color, shape, structure, and size of cells and tissues in each species. Two colors were observed: pinkish red for cellulose cell walls, and green for lignified cell walls. Figures 2, 3, 4, and 5 show the stem and leaf cross-sections studied under the light microscope.

 

Anatomical study of the stem:

The stem cross-sections have a polygonal or circular wavy shape with prominent protuberances forming ribs and grooves. The arrangement of tissues in the three species from the outer surface to the center was the same (Figure 2) starting with an Epidermis; a single layer of circular or oval cellulose epidermal cells surrounded by a cuticle, then a Cortex consists of collenchyma tissue (only in the ribs zone and absence in the groove’s zone), and a thin-walled parenchyma tissue. The Pericycle consists of several layers of small, polygonal sclerenchyma cells, creating a continuous cord surrounding the vascular bundles which are arranged in one ring in the vascular cylinder. Each bundle consists of phloem (red-colored), surrounds the xylem vessels, and xylem (green-colored), includes large secondary vessels and smaller primary ones. In the middle, numerous layers of spongy parenchyma tissue forming the pith, in which the parenchyma cells increase in size towards the center.

 

In R. conglomeratus Murr., the stem cross-section is circular with 10 ribs shaped like a short wide dome, and 10 grooves. The collenchyma type is angular. The mean number of vascular bundles is 28, and a hollow pith exists in the center. Calcium oxalate crystals are present in the pith (Figure 3). 

 

In R. chalepensis Mill., the stem cross-section is polygonal with 8 ribs shaped like a prominent narrow dome, and 8 grooves. The collenchyma type is angular, and the mean number of vascular bundles is 26.

In R. pulcher L., the stem cross-section is polygonal with 8 ribs shaped like a short narrow dome, and 8 grooves that are regularly spaced. The collenchyma tissue is lamellar. The average number of vascular bundles is 19, and there is an absence of cortical parenchyma in the rib's region. Table 2shows a comparison between stem cross-section features in the studied species of Rumex.

 

Figure 2: Stem cross-sections of the three Rumex L. species studied under light microscope.: A1; R. conglomeratus Murr., B1; R. chalepensis Mill., C1; R. pulcher L. at objective magnification (X10), A2; R. conglomeratus Murr., B2; R. chalepensis Mill., C2; R. pulcher L.

 

Figure 3: Druse crystal in the stem cross-section of R. conglomeratus Murr. (X40).

 

Table 2: A comparison between stem cross-section's features in the studied Rumex L. species

Feature	R. conglomeratus	R. chalepensis	R. pulcher.
The shape of stem cross section	Circular	Polygonal	Polygonal
The number of ribs and grooves	10	8	8
Ribs and grooves arrangement	Regular	Regular	Regular
The shape of the ribs	Short and wide dome	Prominent and narrow dome	Short and narrow dome
Cortical parenchyma	present	present	present
Parenchyma layers in groove’s zone	4 – 6	4 – 6	3 – 5
Parenchyma thickness in groove’s zone (mm)	57.7	79.1	38.1
Parenchyma thickness in ribs zone (mm)	23.4	40.9	–
Collenchyma layers	8	9	7
Collenchyma type	Angular	Angular	Lamellar
Internal vascular bundles	Absent	Absent	Absent
Vascular bundles number	28	26 - 27	19
Vascular bundle diameter (mm)	83.5	116.4	73.2
Calcium oxalate crystals	present	absent	absent
Hollow pith	Present	Absent	Absent

 

Anatomical study of the leaf:

Leaf cross-sections of the three species have the same arrangement of tissues (Figure 4), two regions can be noticed, the mesophyll and the middle vessel regions:

 

a)     The mesophyll region between the upper and the lower epidermis, consists of a palisade parenchyma; elongated, rectangular cells positioned next to each other without spaces containing many chloroplasts, and a spongy parenchyma; circular or oval cellulose cells positioned next to each other leaving spaces that allow gas exchange. Numerous rose-shaped calcium oxalate crystals present between the two tissues. Papillary trichomes are present on R. pulcher leaves, and more abundant on the lower side (Figure 5).

 

b)    The middle vessel region, between the upper and lower epidermis, consists of upper and lower collenchyma, and the vascular bundles in the middle surrounded by the parenchyma tissue, each one consists of xylem vessels and phloem. The middle vessel region is less prominent in R. chalepensis than in the other two species (Figure 4). Many differences between leaf cross-sections anatomical features of the studied species were noticed and are presented in Table 3.

 

Table 3: A comparison between leaf cross-section's features of the studied Rumex L. species

Feature	R. conglomeratus Murr.	R. chalepensis Mill.	R. pulcher L.
Palisade parenchyma	Present	Present	Present
Palisade parenchyma layers	3 – 4	2	2 – 3
Spongy parenchyma	Present	Present	Present
Spongy parenchyma layers	1 – 3	3 – 4	3 – 4
Trichomes	Absent	Absent	Present
Calcium oxalate crystals	Present	Present	Present
The number of vascular bundles	3	1	2
Vascular bundle’s diameter (mm)	47.2	65.8	57.2

 

Figure 4: Leaf cross-section of the three Rumex L. species studied: D1; R. conglomeratus Murr., E1; R. chalepensis Mill., F1; R. pulcher L., at objective magnification (X10), D2; R. conglomeratus Murr., E2; R. chalepensis Mill., F2; R. pulcher L. at objective magnification (X40)

 

 

Figure 5: Papillary trichome in R. pulcher ‘s leaf (X40).

 

Statistical analysis:

Mean, max, min, median, and mode for 10 quantitative features of stem and leaf cross-sections were calculated and compared between the three studied species Table 4.

 

The statistical analysis tests revealed significant differences among groups; R. conglomeratus, R. chalepensis, and R. pulcher, for several covariates. Notably, vascular bundle’s diameter (stem), parenchyma thickness in groove’s zone (stem), parenchyma layers (stem), and the number of vascular bundles (leaf) exhibited statistically significant differences among the groups according to the Kruskal-Wallis test (p < 0.05). Collenchyma layers in the stem demonstrated significant differences among the groups according to ANOVA test (p < 0.05).

 

Post-hoc analysis indicated significant differences between specific pairs of groups for the studied covariates, as denoted by the letters 'a', 'b', and 'c' (Table 5). Notably, covariates: vascular bundle’s diameter (leaf), palisade parenchyma layers and spongy parenchyma layers (leaf) showed significant differences between R. conglomeratus and either R. chalepensis or R. pulcher. The lower collenchyma layers (leaf) showed significant differences between R. chalepensis and the other two species, and the number of vascular bundles (stem) of R. pulcher also showed significant differences from the other two species as evidenced by the significant p-values and post-hoc analysis (Table 5).

 

Table 4: The descriptive statistics of some quantitative features in the studied Rumex L. species

The quantitative feature		Species name	Number of measurements	Mean	Max	Min	Median	Mode
Stem cross-sections	Vascular bundle’s diameter (mm)	R. conglomeratus	50	83.5	128.7	42.9	85.8	85.8
		R. chalepensis	50	116.4	165	57.2	114.4	128.7
		R. pulcher	50	73.2	85.8	57.2	71.5	71.5
	The number of vascular bundles	R. conglomeratus	10	28.2	30	27	28	27
		R. chalepensis	10	26.7	29	25	26.5	25
		R. pulcher	10	19	20	18	19	19
	Parenchyma thickness in groove’s zone (mm)	R. conglomeratus	30	57.7	85.8	42.9	57.2	57.2
		R. chalepensis	30	79.1	100.1	71.5	71.5	71.5
		R. pulcher	30	38.1	42.9	28.6	42.9	42.9
	Parenchyma layers	R. conglomeratus	30	5.5	6	4	6	6
		R. chalepensis	30	4.7	6	4	5	5
		R. pulcher	30	4.2	5	3	4	4
	Collenchyma layers	R. conglomeratus	30	7.8	9	6	8	8
		R. chalepensis	30	9.1	11	7	9	10
		R. pulcher	30	7.2	8	5	7	8
Leaf cross-sections	Vascular bundle’s diameter (mm)	R. conglomeratus	10	47.2	57.2	42.9	42.9	42.9
		R. chalepensis	10	65.8	71.5	57.2	71.5	71.5
		R. pulcher	10	57.2	71.5	42.9	57.2	57.2
	The number of vascular bundles	R. conglomeratus	10	2.9	3	2	3	3
		R. chalepensis	10	1	1	1	1	1
		R. pulcher	10	2	2	2	2	2
	Lower collenchyma layers	R. conglomeratus	10	3.4	4	3	3	3
		R. chalepensis	10	1.8	2	1	2	2
		R. pulcher	10	3.6	4	3	4	4
	Palisade parenchyma layers	R. conglomeratus	10	3.4	4	3	3	3
		R. chalepensis	10	2	2	2	2	2
		R. pulcher	10	2.4	3	2	2	2
	Spongy parenchyma layers	R. conglomeratus	10	2.3	3	1	2	2
		R. chalepensis	10	3.5	4	3	3.5	3
		R. pulcher	10	3.3	4	3	3	3

 

Table 5: Kruskal-Walis and ANOVA results of quantitative anatomical features of Rumex L. species studied

Quantitative anatomical feature		ANOVA / Kruskal-Wallis	R. conglomeratus	R. chalepensis	R. pulcher	Test of Homogeneity of Variances (p-value)	Test- Statistic	P-value
			Median (IQR)	Median (IQR)	Median (IQR)
Stem cross-section	Vascular bundle’s diameter	Kruskal-Wallis	85.8 (28.6) bc	114.4 (28.6) ac	71.5 (14.3) ab	-	60.8	0.000
	The number of vascular bundles	ANOVA	28 (1.2) * c	26.7 (1.7) * c	19 (0.8) * ab	0.006	220.900	0.000
	Parenchyma thickness in groove’s zone	Kruskal-Wallis	57.2 (28.6) bc	71.5 (14.3) ac	42.9 (14.3) ab	-	69.276	0.000
	Parenchyma layers	Kruskal-Wallis	6 (1) bc	5 (1) ac	4 (0.25) ab	-	38.431	0.000
	Collenchyma layers	ANOVA	7.8 (0.8)* bc	9.1 (1.2)* ac	7.2 (0.8)* ab	0.051	31.470	0.000
Leaf cross-section	Vascular bundle’s diameter	ANOVA	47.2 (7)* bc	65.8 (7.3)* a	57.2 (9.5)* a	0.849	14.510	0.001
	The number of vascular bundles	Kruskal-Wallis	3 (0.0) bc	1 (0.0) ac	2 (0.0) ab	-	27.692	0.000
	Lower collenchyma layers	Kruskal-Wallis	3 (1) b	2 (0.25) ac	4 (1) b	-	21.608	0.000
	Palisade parenchyma layers	ANOVA	3.4 (0.5)* bc	2 (0.0)* a	2.4 (0.5)* a	0.067	29.250	0.000
	Spongy parenchyma layers	ANOVA	2.3 (0.6)* bc	3.5 (0.5)* a	3 (0.4)* a	0.000	10.230	0.001

*: Used Average (SD) instead of Median (IQR)

a: significant difference with R. conglomeratus, b: significant difference with R. chalepensis, c: significant difference with R. pulcher

DISCUSSION:

The anatomical study of the three Rumex L. species highlighted qualitative and quantitative features of the stem and leaf cross-sections that are of great importance in the identification of plant species ²⁸. The comparison of qualitative features revealed differences among the species. The stem cross-section of R. conglomeratus has a circular, wavy shape, while it is polygonal in R. chalepensis and R. pulcher. In R. pulcher, the shape is more regular, resembling a geometric octagon (Figure 2). The three species also differ in the shape of the rib’s dome; which was the largest and most prominent in R. chalepensis and the least prominent in R. pulcher. R. conglomeratus and R. chalepensis are similar in the angular collenchyma type, whereas R. pulcher has a lamellar collenchyma. The stem of R. conglomereatus is characterized by the presence of calcium oxalate crystals and a hollow pith (Figure 3), which were absent in the stems of the other two species. This differs from the study of keshavarzi et al. because they reported the presence of calcium oxalate crystals in all the species studied except R. elbrusensis ¹⁹. And Soleimani et al. reported the absence of calcium oxalate crystals in the stem of all species studied, and the absence of a hollow pith in all species except R. dentatus ²⁵.

 

The quantitative features measured in the stem cross-sections showed differences between species (refer to Table 4). R. conglomeratus has 10 ribs and 10 grooves, while R. chalepensis and R. pulcher have 8 ribs and 8 grooves. Differences were observed in the parenchyma thickness; it was the highest in R. chalepensis (79.1 mm) and the lowest in R. pulcher (38.1 mm). R. conglomeratus has the largest average number of vascular bundles (28), while R. pulcher has the lowest (19). This indicates the great ability of R. conglomeratus to absorb water, because when the number of vascular bundles increases, the plant’s ability to absorb water also increases ²⁹. The vascular bundle’s diameter was the highest in R. chalepensis (116.4 mm) and the lowest in R. pulcher (73.2 mm). Additionally, the number of collenchyma layers was the highest in R. chalepensis. There are no internal bundles in the medulla of any species. This indicates that the studied species belong to the perennial old form of the genus Rumex L., as mentioned in the study by keshavarzi et al. which is consistent with Joshi ^19,30.

 

The anatomical study of leaf cross-sections revealed that the three species have the same arrangement of tissues in both the middle vessel and mesophyll regions (Figure 4). Characteristic papillary trichomes were observed on the epidermis of R. pulcher leaves (Figure 5), while they were absent in R. conglomeratus and R. chalepensis leaves. The three species differ in the layers of palisade and spongy parenchyma as well as in the number and diameter of the vascular bundles. The palisade parenchyma layers were the highest in R. conglomeratus, while the number of the spongy parenchyma layers were the highest in R. chalepensis. The number of vascular bundles was the highest in R. conglomeratus and the lowest in R. chalepensis. The vascular bundle’s diameter was the highest in R. chalepensis and the lowest in R. conglomeratus.

 

The statistical analysis tests were of a great benefit to find the most important anatomical features that showed significant differences among the three species (Table 5), namely:  vascular bundle’s diameter (stem), parenchyma thickness in groove’s zone (stem), parenchyma layers (stem), collenchyma layers (stem), and the number of vascular bundles (leaf). These features could be of a great importance in the classification of the studied Rumex L. species.

 

CONCLUSION:

This research represents the first detailed anatomical study of leaf cross-sections in three species of Rumex L., namely R. conglomeratus, R. chalepensis, and R. pulcher grown in Syria. It indicated numerous quantitative and qualitative anatomical characteristics of leaves, as well as the anatomical features of the stem cross-sections. The double coloration method was effective in distinguishing the color, shape, structure, and size of cells and tissues using the light microscope. Calcium oxalate crystals were present only in the stem of R. conglomeratus, while the papillary trichomes were found only in the leaf epidermis of R. pulcher. The species have significant differences in the shape of stem and leaf cross-sections and many other qualitative and quantitative features. The number of vascular bundles in leaf cross-section, the shape and number of ribs, the diameter of vascular bundles, the parenchyma layers, the parenchyma thickness in groove’s zone, and the number of collenchyma layers in stem cross-section are of great importance in the classification of the studied Rumex L. species.

 

CONFLICT OF INTEREST:

The authors have no conflicts of interest regarding this investigation.

 

ACKNOWLEDGMENTS:

The authors are grateful to Mrs. Reem Al-Attar for her help to get materials necessary to this study., and to Mr. Nidal Al-Saqqa for performing the statistical analysis.

 

FUNDING INFORMATION:

this research is funded by Damascus University – funder No. 501100020595.

 

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Accepted on 23.10.2024           © RJPT All right reserved

Research J. Pharm. and Tech 2024; 17(11):5235-5241.