Pollen and Seed Morphology as Taxonomic Markers in Verbascum Taxa Based on Herbarium Specimens of MARIUM
Department of Crops and Animal Production, Vocational Higher School of Kızıltepe, Mardin Artuklu University, 47200 Artuklu, Türkiye
Diversity 2024, 16(8), 443; https://doi.org/10.3390/d16080443
Submission received: 22 June 2024
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Revised: 18 July 2024
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Accepted: 23 July 2024
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Published: 26 July 2024
(This article belongs to the Special Issue Herbaria: A Key Resource for Plant Diversity Exploration)
Abstract
:Herbaria are vital resources of biodiversity education and conservation. They contain significant dried collections and botanical data of plant species that are useful for taxonomy, systematics, and plant-based applied research applications. Verbascum L. is the largest genus within the Scrophulariaceae family globally. However, the high morphological diversity within the genus poses significant challenges for accurate species delimitation. This study investigated the pollen and seed morphology of seven distinct Verbascum groups (comprising 10 taxa, including three endemics) from southeastern Anatolia using scanning electron microscopy (SEM). SEM analyses revealed that all examined taxa possessed tricolporate pollen apertures, with pollen shapes varying between prolate spheroidal and oblate spheroidal. Seeds exhibited a light brown to dark brown color, with a prismatic oblong shape and alveolate surface. The seed coat ornamentation consisted of irregular polygonal cells, densely covered with distinct vesicles. Findings demonstrate significant morphological distinctions in both pollen and seed characteristics, suggesting their utility in taxonomic discrimination within Verbascum groups. Notably, the detailed micromorphology revealed by SEM proved to be particularly valuable for classifying these taxa. These results contribute the understanding of the taxonomic diversity within Verbascum and highlight the crucial role of SEM in uncovering microstructural details for accurate species identification.
1. Introduction
Herbaria are vital resources of biodiversity [1,2,3,4]. They have long been used for species descriptions, identification, classification, and estimating geographic ranges [3,5,6]. These data are combined thorough taxonomic monographs and utilized to produce floristic inventories at the local and regional levels [7,8]. Herbarium specimens can serve as baseline data for fundamental and applied research applications [9]. Additionally, herbarium collections and databases are also important for ecology, bioengineering, conservation, food security, and social and cultural aspects of scientific disciplines related to humans [10,11,12,13].
The southeastern Anatolia region is rich in plant diversity. Specifically, Mardin and its surroundings have a rich biodiversity due to the presence of Mediterranean, continental, and desert climates and the altitude between the mountainous and plain parts. Mardin province and its surroundings are among the ancient locations that have been adopted by humanity since the earliest periods of history. However, this historically rich plant biodiversity is under threat due to several reasons, such as unconscious use of pesticides, construction of dams and ponds, excessive and uncontrolled grazing, concretion and destruction of green areas, and industrial facilities. Documentation of floristic composition and preserving dried plant samples grown in this province have significant importance in terms of biodiversity and plant conservation. Therefore, an herbarium titled “Mardin Artuklu University Herbarium” (MARIUM) was established and registered worldwide by Index Herbariorum (https://sweetgum.nybg.org/science/ih/herbarium-details/?irn=264949 (accessed on 1 June 2024)).
The genus Verbascum L., the largest within the Scrophulariaceae family, comprises approximately 360 species globally [14,15]. Turkey, boasting 257 species and 132 hybrid forms, is a hotspot for Verbascum diversity, with 13 artificial groups identified [16,17,18]. Furthermore, Türkiye holds the title of gene center for this genus, hosting an impressive 202 endemic species (80% of the genus’s total endemic taxa) [16,17,19,20,21,22].
The extensive hybridization within Verbascum has led to a high frequency of morphological variation, making species delimitation particularly challenging [16,18]. Consequently, the genus has proven to be taxonomically complex, with identification of taxa often hindered by difficulties in constructing a reliable key. To address these challenges, numerous researchers in Türkiye and internationally have undertaken systematic morphological studies of Verbascum taxa [23].
Previous scanning electron microscopy (SEM) studies have focused on pollen morphology in several Verbascum species [18,23,24,25,26,27,28,29,30,31,32]. Seed micromorphology has also been investigated by several researchers, including Juan et al. [25], Petković et al. [33], Attar et al. [34], Kheiri et al. [35], Karavelioğulları et al. [18,36], Cabi et al. [37], Aytaç and Duman [38], and Duman et al. [39]. However, some gaps remain in our understanding of certain Verbascum taxa, particularly in Türkiye.
This study aimed to investigate the relationships between 10 Verbascum taxa found growing wild in Diyarbakır, Mardin, and Şanlıurfa provinces. This study specifically focused on Verbascum agrimoniifolium subsp. agrimoniifolium, V. orientale subsp. orientale (Group A), V. laetum (Group C), V. tenue Murb. (Group F), V. diversifolium Hochst. (Group G), V. geminiflorum (Group I), V. andrusii, V. kotschyi, V. stepporum Hub.-Mor. (Group K), and V. lasianthum (Group L). By utilizing SEM, we aimed to elucidate the fine structure of pollen and seed surfaces, as well as the external morphology of these reproductive structures. The acquired data might contribute to the classification of the genus and provide valuable evidence for taxonomic assessments.
2. Materials and Methods
2.1. Plant Material and Herbaria
Specimens belonging to 10 Verbascum taxa were collected from diverse localities in Diyarbakır, Mardin, and Şanlıurfa provinces between 2022 and 2023. The scientific identities of samples were confirmed by PhD Fatma Mungan Kılıç and Murat Kılıç, and voucher specimens were deposited in Mardin Artuklu University Herbarium (MARIUM), Department of Plants and Animal Production, Vocational Higher School of Kızıltepe, Mardin Artuklu University, Türkiye (Figure 1). Table 1 provides details on collection locations, herbarium numbers, and habitat information for each investigated taxon. Taxonomic descriptions of the plants were assessed according to Davis et al. [17] and Karavelioğulları [21].
2.2. Palynological Investigations
Pollen grains were prepared for both light microscopy (LM) and scanning electron microscopy (SEM) using standard methods described by Erdtman [40]. For LM examination, pollen grains were prepared following Wodehouse‘s [41] standard procedure and observed in glycerin–water under a standard Isolab microscope. A minimum of 30 pollen grains per specimen were analyzed [35,41].
For SEM, pollen grains were treated with distilled water to remove debris and dust, air-dried, and subsequently mounted on stubs using double-sided adhesive tape. The samples were then coated with gold. Photomicrographs were captured using a ZEISS EVO 50 scanning electron microscope (Jena, Germany).
The following pollen parameters were measured for 30 pollen grains per sample under a light microscope: P (polar axis length), E (equatorial diameter), Clg (colpus length), Clt (colpus width), Plg (polar length), Plt (polar width), Ex (exine thickness), and In (intine thickness). The P/E ratio was calculated, and aperture type (Apt) and ornamentation (Or) were also recorded. Pollen terminologies were utilized according to Punt et al. [42]. All measurements are presented as minimum, maximum, and mean values in Table 2, Figure 2.
2.3. Pollen Morphology: Principal Component and Correlation Analyses
To further investigate the relationships between the examined Verbascum taxa based on quantitative pollen characteristics, a principal component analysis (PCA) was conducted. Prior to analysis, the pollen morphology data (Table 2, Figure 3) were standardized to have a mean of 0 and a standard deviation of 1 to account for differences in measurement scales among the variables. The PCA was performed using R version 4.3.1 with the “factoextra” package. The resulting PCA was generated to visualize the distribution of the taxa and the contribution of each pollen trait to the observed variation. Pearson correlation analysis was performed to assess the relationships between pairs of quantitative pollen traits (Figure 4, Table 3).
2.4. Seed Micromorphology Analysis
Mature seeds were initially examined under an Isolab stereomicroscope to ensure their normal size and maturity. Thirty mature seeds were measured to determine the average seed size. For SEM, seed debris was removed by treatment with distilled water, followed by air-drying. The seeds were then mounted on stubs and coated. Photomicrographs were captured using a ZEISS EVO 50 scanning electron microscope.
3. Results
This study investigated the pollen and seed morphology of ten Verbascum taxa, revealing distinct characteristics within the studied species. Table 2 and Figure 2 and Figure 3 summarize the pollen grain features, while Table 4 and Figure 5 present the seed morphology, including size, shape, color, and surface characteristics.
3.1. Pollen Morphology
3.1.1. Size, Symmetry, and Shape
All examined Verbascum species exhibited isopolar and radially symmetrical pollen grains. The shapes ranged from subprolate to prolate spheroidal and oblate spheroidal. Verbascum orientale subsp. orientale exhibited the smallest pollen dimensions (polar axis: 9.34–25.93 µm; equatorial diameter: 6.68–27.16 µm), while V. agrimoniifolium subsp. agrimoniifolium displayed the largest (Table 2, Figure 2 and Figure 3).
3.1.2. Apertures
Predominantly, the Verbascum pollen grains were tricolporate. However, a varying percentage of tricolpate grains were also observed in several taxa, including V. agrimoniifolium subsp. agrimoniifolium (10%), V. andrusii (47%), V. geminiflorum (32%), V. kotschyi (37%), V. laetum (27%), V. lasianthum (20%), V. orientale subsp. orientale (30%), V. diversifolium (14%), V. stepporum (17%), and V. tenue (12%). Colpi were consistently long (6.92–22.58 µm) and wide (1.87–8.92 µm) with distinct, regular margins and acute ends. Pori measurements ranged from 1.88–9.95 µm in length and 2.14–9.02 µm in width. The aperture membrane surface was psilate in V. agrimoniifolium subsp. agrimoniifolium, V. diversifolium, and V. laetum, while it was scabrate in V. andrusii, V. geminiflorum, V. kotschyi, V. lasianthum, V. orientale subsp. orientale, V. stepporum, and V. tenue (Table 2, Figure 2 and Figure 3).
3.1.3. Exine, Intine, and Ornamentation
3.1.4. Pollen Morphology: Principal Component Analysis
The PCA biplot (Figure 4) illustrates the distribution of the ten Verbascum taxa along the first two principal components (PCs), which together explain 61.5% of the total variation in the pollen data. PC1, accounting for 42.3% of the variation, is strongly positively associated with polar length (Plg), polar width (Plt), exine thickness (Ex), and to a lesser extent, equatorial diameter (E) (Figure 4). V. agrimoniifolium subsp. agrimoniifolium occupies a distinct position along this axis, characterized by markedly higher values for these traits, indicating larger pollen grains with thicker exine. Conversely, V. andrusii exhibits a strong positive association with the P/E ratio, reflecting its smaller pollen size and a more elongated shape compared to other species. PC2 explains 19.2% of the variation and is primarily driven by colpus length (Clg), with a positive association, and P/E ratio with a negative association. Species like V. geminiflorum, V. tenue, and V. diversifolium are positioned towards higher values of PC2, reflecting their relatively longer colpi and larger equatorial diameters. In contrast, V. kotschyi, V. stepporum, and V. lasianthum cluster together towards lower PC2 values, indicating relatively shorter colpi and a trend towards more spherical pollen grains. The PCA analysis effectively distinguishes the Verbascum taxa based on their quantitative pollen characteristics, corroborating the observed morphological distinctions. The results suggest that pollen size parameters (Plg, Plt, E) and exine thickness (Ex) are important traits contributing to the separation of these taxa, potentially reflecting adaptations related to pollen dispersal, viability, or pollination strategies.
3.1.5. Pollen Morphology: Correlation Analysis
Pearson correlation analysis (Table 3) revealed significant (p < 0.001) and strong positive correlations between most of the measured pollen traits. The strongest correlation was observed between polar length (Plg) and equatorial diameter (E) (r = 0.9174), followed by correlations between colpus length (Clg) and both polar length (r = 0.8638) and equatorial diameter (r = 0.94). These findings indicate that pollen size parameters tend to covary strongly in these Verbascum taxa.
3.2. Seed Morphology
3.2.1. Seed Size
According to the measurements, the seed dimensions varied significantly among the studied taxa, ranging from 0.41 to 1.70 mm in length and 0.25 to 0.88 mm in width. Similar to the pollen size observations, V. agrimoniifolium subsp. agrimoniifolium displayed the smallest seed dimensions, while V. orientale subsp. orientale exhibited the largest seeds (Table 4, Figure 5).
3.2.2. Seed Shape
3.2.3. Apex of the Seeds
Variations in seed apex morphology were observed among the studied taxa. V. geminiflorum exhibited an obtuse beak, whereas V. agrimoniifolium subsp. agrimoniifolium displayed both acute and truncated beaks. The remaining species, including V. andrusii, V. kotschyi, V. laetum, V. lasianthum, V. orientale subsp. orientale, V. diversifolium, V. stepporum, and V. tenue, consistently possessed truncated beaks (Table 4, Figure 5).
3.2.4. Seed Color
Four distinct seed color categories were observed: light brown (V. diversifolium, V. kotschyi), brown (V. andrusii, V. geminiflorum, V. lasianthum, V. orientale subsp. orientale, V. stepporum), dark brown (V. laetum, V. tenue), and black (V. agrimoniifolium subsp. agrimoniifolium). Notably, V. diversifolium exhibited variation, with seeds ranging from light brown to brown (Table 4, Figure 5).
3.2.5. Seed Ornamentation
4. Discussion
4.1. Essential Role of Herbarium in Taxonomic Studies
The pollen and seed samples used in this study were obtained from Verbascum genus taxa stored in MARIUM. Herbarium specimens can be suitable sources of biological materials (flowers, pollen, fruits, and seeds) that can be assessed in plant morphology and anatomy [44], as well as plant chemicals (e.g., isotopes, heavy metals, biochemical ingredients). Herpin et al. [45], Körner et al. [46], Nielsen et al. [47]. Dentant, Lavergne, and Malécot [48] conducted a summary study of the taxonomy of rock jasmines (Androsace species, Primulaceae species), while Henning et al. [49] introduced a business data distribution implemented in the EDIT Platform for Cyber Taxonomy, which improves the recording and sustainable operation of sample data. We also provided a brief review of the techniques used in the preparation of morphological and anatomical study of herbarium specimens [50] and the morphological diversity of stored herbarium flowers using geometric morphometrics [51].
4.2. Pollen Morphology: A Useful Tool with Limitations
This study examined ten Verbascum taxa, including three endemic species, revealing consistent traits such as isopolar and radially symmetrical pollen grains with subprolate, prolate spheroidal, or oblate spheroidal shapes. The aperture type was predominantly tricolporate, although a varying presence of tricolpate grains was also observed. The exine structure was tectate with a reticulate ornamentation pattern.
These findings largely agree with previous studies on Verbascum pollen that reported the occurrence of both tricolporate and tricolpate apertures within the genus [23,28,29,30,31,32,52,53]. Similarly, variations in pollen shape align with prior observations, highlighting the presence of prolate, subprolate, and oblate spheroidal forms in different Verbascum species [23,28,29,30,31,32,53]. While broad pollen characteristics, such as aperture type and shape, exhibit some variation within Verbascum, they might not be sufficient for clear taxonomic delimitation at lower levels (Figure 6). This aligns with the observations of Pehlivan et al. [54] and Baser [32], who found that relying solely on basic pollen traits observed through light microscopy might not provide strong taxonomic resolution.
4.3. Exine Sculpturing: A Promising Taxonomic Marker
Interestingly, this study revealed a consistent reticulate exine sculpturing pattern across all examined taxa. This is in contrast with some previous studies that observed variations in exine patterns within the genus [29]. The uniformity in exine sculpturing within these studied taxa from southeastern Anatolia could suggest a closer evolutionary relationship among them or a shared adaptation to specific environmental factors.
Focusing on detailed exine sculpturing, as revealed by SEM, appears to be more informative for taxonomic distinctions within Verbascum genus (Figure 4). This approach aligns with the findings of Pehlivan et al. [54] and Baser [32], highlighting the importance of SEM analysis in revealing taxonomically significant micromorphological features.
4.4. Taxonomic Key Based on Qualitative and Quantitative Characters of Pollen
1 + Oblate spheroidal ...........................................................................................................2
1- Pollen grains other than oblate spheroidal....................................................................6
2 + Exine thickness 1.74 μm...............................V. agrimoniifolium subsp. agrimoniifolium
2- Prolate spheroidal ............................................................................................................3
3 + Exine thickness 0.94 μm.................................................................................................4
3- Exine thickness 0.91 μm...................................................................................................5
4 + Oblate spheroidal, P/E ratio 0.91...........................................................V. geminiflorum
4- Prolate spheroidal, P/E ratio 1.02............................................................V. diversifolium
5 + Prolate spheroidal ..........................................................................................V. kotschyi
5- Oblate spheroidal ..............................................................................................V. lateum
6 + Subprolate.......................................................................................................V. andrusii
6- P/E ratio 0.97 ....................................................................................................................7
7 + Oblate spheroidal, P 13.09 μm............................................................................V. tenue
7- Exine thickness 1.09–1.74 μm..........................................................................................8
8 + P 13.16 μm, P/E 0.90....................................................................................V. lasianthum
8- Exine thickness 0.83–1.09 μm..........................................................................................9
9 + Colpus length 8.69 μm, exine thickness 0.97.....................V. orientale subsp. orientale
9- Colpus length10.35 μm, exine thickness 1.09 μm.................................... V. stepporum
4.5. Quantitative Pollen Traits and Species Relationships
The PCA conducted on quantitative pollen data provides valuable insights into the relationships among the examined Verbascum taxa (Figure 4). The separation of species along PC1, primarily driven by pollen size parameters (polar length, polar width, equatorial diameter) and exine thickness, suggests a potential link between these traits and ecological adaptations. For instance, the distinctly larger pollen grains with thicker exine observed in V. agrimoniifolium subsp. agrimoniifolium could be indicative of adaptations for enhanced pollen dispersal, viability in challenging environments, or specific pollination mechanisms. Further investigations into the pollination ecology of this species would be valuable to explore these possibilities.
The positive association of V. andrusii with a higher P/E ratio, reflecting its more elongated pollen shape, presents another interesting finding. This morphological distinction may be linked to specialized pollination strategies, such as adaptation to a particular pollen vector or a more precise pollen deposition mechanism. Examining the pollination biology of V. andrusii in its natural habitat would be crucial to understand the functional significance of its unique pollen morphology.
4.6. Correlations between Pollen Traits
To complement the PCA, we investigated the correlations between quantitative pollen traits. Pearson correlation analysis revealed significant (p < 0.001) and strong positive correlations between most of the measured pollen variables (Table 3). This widespread intercorrelation suggests that pollen morphology in these Verbascum taxa is often characterized by coordinated changes in multiple size parameters. For instance, the very strong positive correlation (r = 0.9174) between polar length (Plg) and equatorial diameter (E) indicates that pollen grains with greater length also tend to have greater width, reflecting an overall larger size. This pattern is further supported by the strong positive correlations observed between colpus length (Clg) and both Plg and E.
The prevalence of such correlations could be indicative of shared developmental pathways influencing these traits or selective pressures favoring particular combinations of pollen size parameters. For example, larger pollen grains, with their increased surface area, might have an advantage in pollen hydration or nutrient storage, potentially impacting pollen viability or interactions with pollinators. Further research, incorporating ecological data and experimental manipulations, would be needed to unravel the functional significance of these correlated traits.
4.7. Seed Morphology and Taxonomic Significance in Verbascum
This study utilized SEM and stereomicroscopy to examine the seed morphology of Verbascum species, confirming the effectiveness of this approach in highlighting taxonomically significant characteristics. Findings align with previous research emphasizing the importance of micromorphology and ornamentation in fruit and seed for taxonomic studies within this genus [32,55].
Observations revealed consistent features within the studied taxa, including a color range of light brown to black upon maturity. This finding corroborates the dark brown to black seed coloration reported by Attar et al. [34] and Cabi et al. [37]. However, it is important to acknowledge that seed color can be influenced by various factors, including genetic variation and environmental conditions during seed development.
Seed size exhibited some variation within the studied taxa, ranging from 0.41 to 1.70 mm in length and 0.25 to 0.88 mm in width (Figure 7 and Figure 8). This observation aligns with Attar et al. [34], who reported size variations among and within populations, even within the same capsule. However, this study design, like those previously mentioned, had limitations in capturing the full spectrum of size variation due to the limited number of populations and individuals examined.
Comparing seed size measurements (V. agrimoniifolium subsp. agrimoniifolium—0.51 × 0.31 mm, V. orientale subsp. orientale—1.40 × 0.56 mm) with previous studies [34,37] revealed general agreement. However, discrepancies were observed with measurements reported by Baser [32], where measurements were consistently larger. These differences could be attributed to several factors, including geographic variation, genetic differences between studied populations, and variations in measurement methodologies. Further investigation into these discrepancies could provide valuable insights into the factors influencing seed size variation in Verbascum.
Interestingly, this study confirmed the observations of Baser [32] regarding the taxonomic utility of seed shape in Verbascum. The results demonstrated distinct variations in seed shape, not just between species, but also between subspecies within V. orientale. Specifically, V. orientale subsp. orientale had the longest seeds, while V. agrimoniifolium subsp. agrimoniifolium had the smallest. This finding highlights the potential of seed morphology, particularly shape, as a valuable tool for species and subspecies identification within this genus.
Further research incorporating a broader sampling strategy across different populations and environmental gradients is needed to strengthen understanding of the taxonomic significance of seed features in Verbascum. Combining morphometric analyses with molecular techniques would provide a more robust framework for resolving taxonomic uncertainties and understanding the evolutionary relationships within this diverse genus.
4.8. Taxonomic Key Based on Qualitative and Quantitative Morphological Features of Seed
1 + Seed shape prismatic, elliptic to oblong...........V. agrimoniifolium subsp. agrimoniifolium
1- Seed shape prismatic ovate and oblong................................................................................2
2 + Seed shape truncated beak, L/W ratio 1.47.........................................................V. andrusii
2- Seed shape obtuse beak..........................................................................................................3
3 + Seed striped from apex to hilum, L/W ratio 1.63 .......................................V. geminiflorum
3- Seed in approximately striped from apex to hilu................................................................4
4 + Seed shallow alveolate, ± deep and broad ridges..............................................V. kotschyi
4- Seed striped between apex and hilum..................................................................................5
5 + Seed surface irregular, with small rectangular cells ...........................................V. laetum
5- Seed surface irregular with polygonal cells.........................................................................6
6 + Seed shape prismatic and oblong, L/W ratio 1.56 ...........................................V. lasianthum
6- Seed shape prismatic, elliptic to oblong and like a boot with...........................................7
7 + Seed surface irregular small with cells .....................................V. orientale subsp. orientale
7- Seed often with truncated beak, and some with broad beak................................................8
8 + Seed color light brown-brown, L/W ratio 1.64 ............................................V. diversifolium
8- Seed color brown, shape prismatic-oblong..........................................................................9
9 + Seed surface irregular polygonal cells, L/W ratio 1.46 ....................................V. stepporum
9- Seed surface with densely and indistinct vesicles.............................................................10
10 + Seed shape reniform, dark brown, L/W 1.96 ........................................................V. tenue
5. Conclusions
Pollen and seed samples from Verbascum taxa housed in the MARIUM herbarium were utilized in this study. The value of herbarium collections as reliable sources of biological material for plant micromorphology and palynology research was demonstrated. Furthermore, such collections are recognized as essential for documenting, expanding, and preserving taxonomic knowledge.
These findings underscore the taxonomic value of seed and pollen morphology in Verbascum. This study reveals that morphological differences in seed and pollen characteristics, such as size, shape and ornamentation can be effectively employed for both interspecific and infraspecific discrimination within the genus. Specifically, the results highlight the potential of seed and pollen morphology for distinguishing between closely related species and even subspecies within Verbascum. This reinforces the importance of incorporating detailed seed and pollen morphological analyzes in future taxonomic revisions and identification keys for this genus.
Funding
This research was funded by [Project Coordination of Mardin Artuklu University] grant number [MAÜ.BAP.22.KMY.011] and The APC was funded by [Fatma MUNGAN KILIÇ].
Institutional Review Board Statement
Not applicable.
Data Availability Statement
The data supporting the findings of this study are presented within the article.
Acknowledgments
This research was supported by the Scientific Investigation Project Coordination of Mardin Artuklu University [grant number MAÜ.BAP.22.KMY.011]. The author gratefully acknowledges the financial support provided by this grant. The author also grateful to Seed Technology and Genetics Application and Research Center and Mardin Artuklu University Herbarium (MARIUM) for their technical support. The author extends sincere thanks to Veysel YILDIZ for their invaluable technical assistance with scanning electron microscopy and photography. The author extends sincere thanks to Associate Professor Enver KENDAL for their invaluable technical assistance with principal component analysis (PCA). Special appreciation is also extended to Associate Professor Mehmet Maruf BALOS, Cahit ÇEÇEN (Şanlıurfa), and Murat KILIÇ (Diyarbakır, Mardin, Şanlıurfa) for their generous contributions to field studies and species collection.
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1.
Appearance of the Verbascum taxa used in this study in their wild habitats and their herbaria in MARIUM. In the genus Verbascum. 1—Habitat; 2—Herbaria. (a1,a2) V. agrimoniifolium subsp. agrimoniifolium; (b1,b2) V. andrusii; (c1,c2) V. geminiflorum; (d1,d2) V. kotschyi; (e1,e2) V. laetum; (f1,f2) V. lasianthum; (g1,g2) V. orientale subsp. orientale, (h1,h2) V. stepporum; (i1,i2) V. tenue; (j1,j2) V. diversifolium (Specimen from Kew Herbarium—K000975933).
Figure 1.
Appearance of the Verbascum taxa used in this study in their wild habitats and their herbaria in MARIUM. In the genus Verbascum. 1—Habitat; 2—Herbaria. (a1,a2) V. agrimoniifolium subsp. agrimoniifolium; (b1,b2) V. andrusii; (c1,c2) V. geminiflorum; (d1,d2) V. kotschyi; (e1,e2) V. laetum; (f1,f2) V. lasianthum; (g1,g2) V. orientale subsp. orientale, (h1,h2) V. stepporum; (i1,i2) V. tenue; (j1,j2) V. diversifolium (Specimen from Kew Herbarium—K000975933).
Figure 2.
Scanning electron micrographs of pollen grains in the genus Verbascum. 1—equatorial view; 2—exine sculpturing. (a1,a2) V. agrimoniifolium subsp. agrimoniifolium; (b1,b2) V. andrusii; (c1,c2) V. geminiflorum; (d1,d2) V. kotschyi; (e1,e2) V. laetum; (f1,f2) V. lasianthum; (g1,g2) V. orientale subsp. orientale; (h1,h2) V. diversifolium; (i1,i2) V. stepporum; (j1,j2) V. tenue.
Figure 2.
Scanning electron micrographs of pollen grains in the genus Verbascum. 1—equatorial view; 2—exine sculpturing. (a1,a2) V. agrimoniifolium subsp. agrimoniifolium; (b1,b2) V. andrusii; (c1,c2) V. geminiflorum; (d1,d2) V. kotschyi; (e1,e2) V. laetum; (f1,f2) V. lasianthum; (g1,g2) V. orientale subsp. orientale; (h1,h2) V. diversifolium; (i1,i2) V. stepporum; (j1,j2) V. tenue.
Figure 3.
Light microscopy micrographs of pollen grains from representative Verbascum taxa. (a) V. agrimoniifolium subsp. agrimoniifolium, (b) V. andrusii, (c) V. geminiflorum, (d) V. kotschyi, (e) V. laetum, (f) V. lasianthum, (g) V. orientale subsp. orientale, (h) V. diversifolium, (i) V. stepporum, (j) V. tenue.
Figure 3.
Light microscopy micrographs of pollen grains from representative Verbascum taxa. (a) V. agrimoniifolium subsp. agrimoniifolium, (b) V. andrusii, (c) V. geminiflorum, (d) V. kotschyi, (e) V. laetum, (f) V. lasianthum, (g) V. orientale subsp. orientale, (h) V. diversifolium, (i) V. stepporum, (j) V. tenue.
Figure 4.
Principal component analysis (PCA) biplot of ten Verbascum taxa based on quantitative pollen morphology data. Each point represents a species, and the position of the species on the plot reflects its pollen characteristics. The arrows represent pollen traits and their contribution to the principal components (PCs). Closer proximity between species on the plot suggests greater similarity in their pollen morphology.
Figure 4.
Principal component analysis (PCA) biplot of ten Verbascum taxa based on quantitative pollen morphology data. Each point represents a species, and the position of the species on the plot reflects its pollen characteristics. The arrows represent pollen traits and their contribution to the principal components (PCs). Closer proximity between species on the plot suggests greater similarity in their pollen morphology.
Figure 5.
Scanning electron micrographs of seeds in the genus Verbascum. 1—general appearance; 2—surface ornamentation. (A1,A2) V. agrimoniifolium subsp. agrimoniifolium; (B1,B2) V. andrusii; (C1,C2) V. geminiflorum; (D1,D2) V. kotschyi; (E1,E2) V. laetum; (F1,F2) V. lasianthum; (G1,G2) V. orientale subsp. orientale; (H1,H2) V. diversifolium; (I1,I2) V. stepporum; (J1,J2) V. tenue.
Figure 5.
Scanning electron micrographs of seeds in the genus Verbascum. 1—general appearance; 2—surface ornamentation. (A1,A2) V. agrimoniifolium subsp. agrimoniifolium; (B1,B2) V. andrusii; (C1,C2) V. geminiflorum; (D1,D2) V. kotschyi; (E1,E2) V. laetum; (F1,F2) V. lasianthum; (G1,G2) V. orientale subsp. orientale; (H1,H2) V. diversifolium; (I1,I2) V. stepporum; (J1,J2) V. tenue.
Figure 6.
Colpus length, P/E ratio, and exine thickness of investigated taxa of Verbascum.
Figure 7.
Seed size (mm) variation in studied Verbascum taxa.
Figure 8.
Seed length-to-width ratios in Verbascum species.
Table 1.
Verbascum species used for morphology studies and collected localities.
| Species | Group | Collection Areas and Habitat | Date | Altitude (m) | Coordinates | Collector | Herbarium No (MARIUM) |
|---|---|---|---|---|---|---|---|
| V. agrimoniifolium subsp. agrimoniifolium | A | C8 Diyarbakır: Siverek-Diyarbakır road, 35 km from Diyarbakır, roadside, rocky slope | 2 June 2022 | 1014 | Not available | F Mungan Kılıç M.Kılıç | 1 |
| C8 Mardin: Artuklu, roadside | 5 June 2022 | 971 | 37°22′22″ N 40°42′11″ E | F Mungan Kılıç M.Kılıç | 2 | ||
| C7 Şanlıurfa: Karaköprü, roadside | 19 May 2022 | 554 | 37°11′22″ N 38°48′49″ E | F Mungan Kılıç M.Kılıç | 3 | ||
| V. andrusii | K | Mardin: Artuklu, roadside | 9 May 2022 | 695 | 37°17′46″ N 40°42′47″ E | F Mungan Kılıç M.Kılıç | 4 |
| Mardin: Nusaybin, roadside | 21 May 2022 | 536 | 37°08′11″ N 41°04′44″ E | F Mungan Kılıç M.Kılıç | 5 | ||
| Mardin: Ömerli, roadside | 24 May 2022 | 774 | 37°23′58″ N 38°52′13″ E | F Mungan Kılıç M.Kılıç | 6 | ||
| Mardin: Midyat, roadside | 24 May 2022 | 1001 | 37°28′15″ N 41°07′18″ E | F Mungan Kılıç M.Kılıç | 7 | ||
| Mardin: Dargeçit, roadside | 24 May 2022 | 933 | 37°33′08″ N 41°40′16″ E | F Mungan Kılıç M.Kılıç | 6 | ||
| Mardin: Kızıltepe, roadside | 28 May 2022 | 655 | 37°16′31″ N 40°32′41″ E | F Mungan Kılıç M.Kılıç | 7 | ||
| Mardin: Yeşilli, roadside | 29 May 2022 | 733 | 37°18′31″ N 40°49’54″ E | F Mungan Kılıç M.Kılıç | 8 | ||
| V. geminiflorum | I | Mardin: Artuklu, roadside | 16 May 2022 | 591 | 37°16’22″ N 40°40’49″ E | F Mungan Kılıç M.Kılıç | 9 |
| Şanlıurfa: Siverek, roadside | 2 June 2022 | 867 | 37°43’30″ N 39°25’05″ E | F Mungan Kılıç M.Kılıç | 10 | ||
| V. kotschyi | K | Mardin: Artuklu, roadside | 10 May 2022 | 828 | 37°19’38″ N 40°47’48″ E | F Mungan Kılıç M.Kılıç | 11 |
| Mardin: Nusaybin, roadside | 21 May 2022 | 546 | 37°08’06″ N 41°04’41″ E | F Mungan Kılıç M.Kılıç | 12 | ||
| Mardin: Yeşilli, roadside | 24 May 2022 | 1158 | 37°22’17″ N 40°51’38″ E | F Mungan Kılıç M.Kılıç | 13 | ||
| Mardin: Savur, roadside | 31 May 2022 | 1113 | 37°31’10″ N 40°55’56″ E | F Mungan Kılıç M.Kılıç | 14 | ||
| Şanlıurfa: Karaköprü, roadside | 2 August 2022 | 621 m | 37°12′34″ N 38°47′28″ E | F Mungan Kılıç M.Kılıç | 15 | ||
| V. laetum | C | Mardin: Artuklu, roadside | 24 April 2022 | 848 | 37°20′12″ N 40°46′26″ E | F Mungan Kılıç M.Kılıç | 16 |
| Mardin: Mazıdağı, roadside | 15 May 2022 | 939 | 37°30′14″ N 40°31′19″ E | F Mungan Kılıç M.Kılıç | 17 | ||
| Mardin: Midyat, roadside | 24 May 2022 | 928 | 37°26′15″ N 41°18′07″ E | F Mungan Kılıç M.Kılıç | 18 | ||
| Mardin: Savur, roadside | 31 May 2022 | 933 | 37°31′31″ N 40°53′37″ E | F Mungan Kılıç M.Kılıç | 19 | ||
| Şanlıurfa: Viranşehir-Urfa road, 25 km after Viranşehir, roadside, stony slopes | 19 May 2022 | - | Not available | F Mungan Kılıç M.Kılıç | 20 | ||
| V. lasianthum | L | Diyarbakır: Çınar, roadside | 2 June 2022 | 725 | 37°40′47″ N 40°27′28″ E | F Mungan Kılıç M.Kılıç | 21 |
| Diyarbakır: Yenişehir, 28 km from Ergani, roadside, cultivated fields | 2 June 2022 | 766 | Not available | F Mungan Kılıç M.Kılıç | 22 | ||
| Diyarbakır: Ergani, roadside | 2 June 2022 | 809 | 38°11′53″ N 39°49′57″ E | F Mungan Kılıç M.Kılıç | 23 | ||
| Mardin: Yeşilli, roadside | 29 May 2022 | 676 | 37°16′53″ N 40°50′46″ E | F Mungan Kılıç M.Kılıç | 24 | ||
| Mardin: Savur, roadside | 31 May 2022 | 903 | 37°29′05″ N 40°49′40″ E | F Mungan Kılıç M.Kılıç | 25 | ||
| Mardin: Artuklu, roadside | 3 August 2022 | 1132 | 37°22′55″ N 40°39′07″ E | F Mungan Kılıç M.Kılıç | 26 | ||
| Mardin: Ömerli, 6 km after Ömerli, the roadside | 4 August 2022 | - | Not available | F Mungan Kılıç M.Kılıç | 27 | ||
| Şanlıurfa: Karaköprü, roadside | 19 May 2022 | 665 | 37°13′46″ N 38°49′06″ E | F Mungan Kılıç M.Kılıç | 28 | ||
| Şanlıurfa: Hilvan, Near Hilvan location, roadside | 2 August 2022 | 592 | Not available | F Mungan Kılıç M.Kılıç | 29 | ||
| V. orientale subsp. orientale | A | Mardin: Artuklu, roadside | 13 May 2022 | 835 | 37°20′44″ N 40°43′44″ E | F Mungan Kılıç M.Kılıç | 30 |
| V. diversifolium (E) | G | Türkiye, C7 Şanlıurfa: Siverek, Hilvan-Siverek road, 29 km from Siverek, the roadside cultivated area | 2 August 2022 | 604 | 37°36′32″ N 39°05′19″ E | F Mungan Kılıç M.Kılıç | 31 |
| V. stepporum (E) | K | Şanlıurfa: Viranşehir-Urfa road, roadside right–left stony area, around the highway (400-26/042) sign | 19 May 2022 | 660 | Not available | F Mungan Kılıç M.Kılıç | 32 |
| Şanlıurfa: Haliliye, North of Güzelyurt village, roadside | 19 May 2022 | 665 | 37°12′49″ K 38°49′05″ D | F Mungan Kılıç M.Kılıç | 33 | ||
| Şanlıurfa: Karaköprü, Borsa İstanbul Secondary School south, roadside | 19 May 2022 | 606 | 37°12′26″ K 38°47′30″ D | F Mungan Kılıç M.Kılıç | 34 | ||
| Şanlıurfa: Karaköprü, Gölpınar Nature Park south, roadside | 19 May 2022 | 704 | 37°14′05″ K 38°49′30″ D | F Mungan Kılıç M.Kılıç | 35 | ||
| Şanlıurfa: Bozova, Yassıca recreation area | 19 May 2022 | 553 | 37°27′25″ K 38°23′26″ D | M Balos C Çeçen | 36 | ||
| Şanlıurfa: Hilvan, 24 km from Hilvan, the roadside cultivated area | 2 August 2022 | 774 | 37°23′58″ K 38°52′13″ D | F Mungan Kılıç M.Kılıç | 37 | ||
| V. tenue (E) | F | Şanlıurfa: Şanlıurfa-Adıyaman highway, Mardin, Habur junction, roadside, calcareous slope | 19 May 2022 | 717 | 37°11′55″ K 38°48′01″ D | F Mungan Kılıç M.Kılıç | 38 |
| Şanlıurfa: Bozova, Şanlıurfa-Bozova road, before reaching Bozova, opposite Opet, by the roadside | 19 May 2022 | 616 | 37°20′40″ K 38°32′02″ D | M Balos C Çeçen | 39 |
Table 2.
Pollen morphological characters in species of Verbascum (µm).
| Species | P min (Mean) Max | E min (Mean) Max | P/E Ratio | Shape | Clg min (Mean) Max | Clt Min (Mean) Max | Plg Min (Mean) Max | Plt Min (Mean) Max | Ex Min (Mean) Max | In Min (Mean) Max | Apt | Or |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| V. agrimoniifolium subsp. agrimoniifolium | 21.71 (23.15) 25.93 | 22.11 (24.85) 27.16 | 0.93 | Oblate spheroidal | 17.15 (18.94) 22.58 | 4.72 (6.65) 8.92 | 6.33 (7.75) 9.95 | 5.12 (6.89) 9.02 | 1.32 (1.74) 2.30 | 0.73 (0.93) 1.40 | 90% Tricolporate 10% Tricolpate | Reticulate |
| V. andrusii | 11.08 (12.88) 14.36 | 6.68 (8.34) 11.78 | 1.54 | Subprolate | 8.09 (9.80) 11.47 | 2.00 (3.12) 4.44 | 3.15 (3.72) 4.55 | 2.19 (3.05) 4.89 | 0.56 (0.83) 1.03 | 0.30 (0.48) 0.70 | 53% Tricolporate 47% Tricolpate | Reticulate |
| V. geminiflorum | 12.25 (13.31) 14.66 | 13.53 (14.52) 15.21 | 0.91 | Oblate spheroidal | 9.30 (11.05) 12.66 | 2.51 (3.19) 3.75 | 2.53 (3.47) 4.22 | 3.09 (3.88) 4.62 | 0.64 (0.94) 1.11 | 0.35 (0.53) 0.75 | 68% Tricolporate 32% Tricolpate | Reticulate |
| V. kotschyi | 12.22 (13.81) 17.09 | 10.39 (13.73) 15.83 | 1.01 | Prolate spheroidal | 9.19 (11.17) 14.84 | 1.91 (3.03) 4.36 | 3.59 (4.42) 5.82 | 2.64 (3.57) 4.35 | 0.69 (0.91) 1.15 | 0.35 (0.52) 0.64 | 63% Tricolporate 37% Tricolpate | Microreticulate |
| V. laetum | 9.75 (11.08) 12.91 | 9.67 (11.33) 13.58 | 0.97 | Oblate spheroidal | 7.80 (9.07) 10.89 | 1.87 (2.86) 3.99 | 2.44 (3.86) 5.09 | 2.25 (3.31) 4.88 | 0.71 (0.91) 1.13 | 0.32 (0.48) 0.60 | 73% Tricolporate 27% Tricolpate | Reticulate |
| V. lasianthum | 10.27 (13.16) 15.41 | 10.85 (14.66) 17.45 | 0.90 | Oblate spheroidal | 7.74 (10.45) 12.78 | 2.68 (3.84) 4.97 | 3.44 (4.81) 5.88 | 2.78 (4.06) 5.13 | 0.71 (1.14) 1.54 | 0.45 (0.64) 0.88 | 80% Tricolporate 20% Tricolpate | Microreticulate |
| V. orientale subsp. orientale | 9.34 (11.03) 13.42 | 8.53 (11.68) 14.89 | 0.94 | Oblate spheroidal | 6.92 (8.69) 11.17 | 2.20 (2.93) 3.89 | 2.83 (3.94) 4.73 | 2.76 (3.33) 4.07 | 0.75 (1.09) 1.40 | 0.32 (0.52) 0.66 | 70% Tricolporate 30% Tricolpate | Reticulate |
| V. diversifolium | 11.79 (13.27) 15.87 | 11.83 (12.99) 15.17 | 1.02 | Prolate spheroidal | 8.74 (10.64) 13.44 | 2.02 (2.70) 3.80 | 1.88 (2.77) 3.71 | 2.14 (3.10) 3.88 | 0.71 (0.94) 1.24 | 0.32 (0.46) 0.64 | 86% Tricolporate 14% Tricolpate | Reticulate |
| V. stepporum | 11.60 (13.55) 17.23 | 10.71 (12.60) 14.40 | 1.08 | Prolate spheroidal | 8.02 (10.35) 14.77 | 2.06 (3.02) 4.03 | 3.23 (4.43) 6.53 | 2.98 (3.88) 4.86 | 0.64 (0.97) 1.25 | 0.27 (0.48) 0.70 | 83% Tricolporate 17% Tricolpate | Reticulate |
| V. tenue | 11.23 (13.09) 15.57 | 12.20 (13.42) 15.27 | 0.97 | Oblate spheroidal | 9.12 (10.27) 12.15 | 2.01 (2.99) 4.20 | 3.39 (4.46) 6.35 | 2.26 (3.67) 4.59 | 0.56 (1.00) 1.50 | 0.32 (0.57) 0.78 | 88% Tricolporate 12% Tricolpate | Reticulate |
P: polar axis length; E: equatorial diameter; Clg: colpus length; Clt: colpus width; Plg: polar length; Plt: polar width; Ex: exine thickness; In: intine thickness; Apt: aperture type; Or: ornamentation.
Table 3.
Pearson correlation coefficients (r) between quantitative pollen traits in ten Verbascum taxa. Values shown are correlation coefficients. ** represent Significance levels: p < 0.001 (highly significant).
Table 3.
Pearson correlation coefficients (r) between quantitative pollen traits in ten Verbascum taxa. Values shown are correlation coefficients. ** represent Significance levels: p < 0.001 (highly significant).
| P | E | P/E | Clg | Clt | Plg | Plt | Ex | |
|---|---|---|---|---|---|---|---|---|
| E | 0.9174 ** | |||||||
| P/E | −0.1405 | −0.5184 | ||||||
| Clg | 0.9948 ** | 0.94 | −0.2051 | |||||
| Clt | 0.9455 | 0.911 ** | −0.2037 | 0.9458 ** | ||||
| Plg | 0.8756 | 0.857 | −0.2384 | 0.8638 ** | 0.9348 | |||
| Plt | 0.9482 ** | 0.9586 ** | −0.3376 | 0.9528 ** | 0.9732 ** | 0.9419 ** | ||
| Ex | 0.8822 ** | 0.9268 ** | −0.3909 | 0.8857 ** | 0.9528 ** | 0.9115 ** | 0.9508 ** | |
| In | 0.9039 ** | 0.9289 ** | −0.3323 | 0.9092 ** | 0.9755 ** | 0.9418 ** | 0.9618 ** | 0.9639 ** |
Table 4.
Seed morphological characteristics in Verbascum taxa (mm).
| Species | Group | Length Min (Mean) Max | Width Min (Mean) Max | Color | Shape | Seed Surface |
|---|---|---|---|---|---|---|
| V. agrimoniifolium subsp. agrimoniifolium | A | 0.41 (0.51) 0.62 | 0.25 (0.31) 0.37 | Black | Prismatic and oblong with shallow alveolate, truncated and acute beaks. | Irregular rectangular cells, with densely and distinct vesicles. |
| V. andrusii | K | 0.66 (0.94) 1.26 | 0.48 (0.64) 0.81 | Brown | Prismatic ovate and oblong with ±shallow alveolate, deep and broad ridges, truncated beaks. | Irregular polygonal cells, with densely and distinct vesicles. |
| V. geminiflorum | I | 0.75 (1.04) 1.63 | 0.37 (0.64) 0.86 | Brown | Prismatic ovate and oblong with ±shallow alveolate, obtuse beaks, striped from apex to hilum. | Irregular polygonal cells, with densely and distinct vesicles. |
| V. kotschyi | K | 0.80 (1.16) 1.60 | 0.51 (0.69) 0.88 | Light brown | Prismatic ovate and oblong with shallow alveolate, ±deep and broad ridges, truncated beaks, approximately striped from apex to hilum. | Irregular polygonal cells, with densely and distinct vesicles. |
| V. laetum | C | 0.53 (0.86) 1.10 | 0.39 (0.59) 0.83 | Dark brown | Prismatic, prismatic ovate and oblong with ±shallow alveolate, truncated beaks, striped between apex and hilum. | Irregular and exserted rectangular cells with vesicles only on the angles of the walls cells. |
| V. lasianthum | L | 0.49 (0.70) 1.01 | 0.29 (0.45) 0.59 | Brown | Prismatic and oblong with ±shallow alveolate, deep ridges, truncated beaks, striped from apex to hilum. | Irregular polygonal cells, with densely and distinct vesicles. |
| V. orientale subsp. orientale | A | 1.01 (1.40) 1.70 | 0.32 (0.56) 0.80 | Brown | Prismatic, elliptic to oblong and like a boot with ±shallow alveolate, deep ridges, truncated beaks. | Irregular small rectangular cells, with densely and distinct vesicles. |
| V. diversifolium (E) | G | 0.58 (0.92) 1.20 | 0.33 (0.56) 0.72 | Light brown-brown | Prismatic oblong with ±shallow alveolate, often with truncated beaks, and some with broad beaks | Irregular polygonal cells, with densely and distinct vesicles |
| V. stepporum (E) | K | 0.63 (0.79) 1.00 | 0.30 (0.54) 0.70 | Brown | Prismatic oblong with ±shallow alveolate, truncated beak | Irregular polygonal cells, with densely and distinct vesicles |
| V. tenue (E) | F | 0.75 (1.12) 1.34 | 0.38 (0.57) 0.84 | Dark brown | Prismatic oblong and reniform with shallow alveolate, truncated beak | Irregular polygonal cells, with densely and indistinct vesicles |
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Mungan Kılıç, F. Pollen and Seed Morphology as Taxonomic Markers in Verbascum Taxa Based on Herbarium Specimens of MARIUM. Diversity 2024, 16, 443. https://doi.org/10.3390/d16080443
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Mungan Kılıç F. Pollen and Seed Morphology as Taxonomic Markers in Verbascum Taxa Based on Herbarium Specimens of MARIUM. Diversity. 2024; 16(8):443. https://doi.org/10.3390/d16080443
Chicago/Turabian StyleMungan Kılıç, Fatma. 2024. "Pollen and Seed Morphology as Taxonomic Markers in Verbascum Taxa Based on Herbarium Specimens of MARIUM" Diversity 16, no. 8: 443. https://doi.org/10.3390/d16080443
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