Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan

Kaleem Ullah Kakar, et al., BAOJ Biotech 2016, 2: 12: 009

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Kaleem Ullah Kakar1, 3, Raqeeb Ullah5, Zarqa Nawaz1, 2, 4*, Muhammad Ishtiaq4, Faizan Ullah4, Syed Anil Gilani4, Robina Shaheen4, Kokab Satti6 and Rizwana Aleem Qureshi4*

1China Tobacco Key Laboratory of Molecular Genetics, Guizhou Academy of Tobacco Science, 550081, Guiyang City, Guizhou Province, China2Wuxi Hupper BioSeed technology Company, Jiangsu Province, 21000 China

3State Key Laboratory of Rice Biology, Institute of Crop Science, Zhejiang University, Hangzhou, 310029, China4Quaid –i- Azam University, Department of Plant Sciences, Islamabad

5Quaid –i- Azam University, Department of Environmental Sciences, Islamabad6PARC Institute of Advanced studies in Agriculture, NARC, Islamabad

BAOJ Biotechnology

*Corresponding author: Zarqa Nawaz, China Tobacco Key Laboratory of Molecular Genetics, Guizhou Academy of Tobacco Science, 550081, Guiyang City, Guizhou Province, China, Tel: +86-18786003752; E-mail: zarqanawaz@zju.edu.cn

Rizwana Aleem Qureshi, Azam University, Department of Plant Sciences, Islamabad, Pakistan, E-mail: rizwanaaleem@yahoo.com

Sub Date: February 8, 2016, Acc Date: March 12, 2016, Pub Date: March 14, 2016

Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

Copyright: © 2016 Kaleem Ullah Kakar, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Research Article

AbstractDraba L. is considered taxonomically the most difficult and important genus of family Brassicaceae. Keeping in mind the importance of the taxon, palynological studies of nineteen species of Draba from Pakistan was carried out using light and electron microscopy. Despite nearly half a century of research, the systematic relationships among species in the genus Draba remain unresolved. In this study we analyzed pollen morphology and examined how variations in key pollen characteristics relate to our current understanding of the taxonomy of this genus. Palynological studies are known to aid in the morphological studies and classification of a taxon. The results show that the pollen grains of Draba species studied are usually radially symmetrical, isopolar sub-prolate to prolate, or prolate-spheroidal, tricolpate, reticulte exine sculpturing and long sunken apertures. Along with these qualitative features some qualitative characters like size of the pollen, equatorial length and diameter, polar length and diameter, number of colpi, colpus length, distance between apertures and exine thickness were also studied. Analysis of variance (ANOVA) exhibited the significance of these results. Moreover, hierarchical analysis was also carried out on the basis of quantitative characters to see the interspecies relationship among the taxa under study. Cluster analysis showed that nineteen species of this genus belong to two distinct clades. Groupings based on pollen characteristics alone aligned completely with those based on all morphological data supporting the current systematic treatment of the genus.

Keywords: Draba, Brassicaceae; Pollen Morphology; Light and Electron Microscopy; Pakistan.

IntroductionThe family Brassicaceae, also known as Cruciferae is one of the largest families of the Angiosperms with more than 330 genera and above 3500 species found in all continents except Antarctica, mainly in temperate areas, with highest diversity in Irano-Turanian, Mediterranean, and W. North American regions. Of these only 92 genera and about 250 species are reported from Pakistan and among these, 5 genera and 14 species are cultivated [1]. Draba is

a natural group of family Brassicaceae, with rich species diversity [2]. It is the largest and taxonomically the most complex genus of the family bearing more than 950 binomials and several infra specific taxa [3]. It is distinctly separated from other genera of the family Brassicaceae by: indumentum type, latiseptate siliculae, biseriate seeds, accumbent dicotyledons etc [4-8]. Schulz [4] recognized about 210 species of the genus Draba world over which have increased up to 400 species by now. The genus is distributed in the Arctic, subarctic, alpine and most mountainous regions of the world. About 90 species of Draba occur in Russia, 70 species in South America, 43 species in Europe, 48 species in China, 37 species in India, 24 species in Nepal, 17 species in Turkey, and 10 species in Afghanistan [9]. However this number is increasing rapidly with the report of new species from these areas. Draba laegaardii Al-Shehbaz is the latest member from South America [10]. Hooker [11] described 12 species of the genus Draba in British Indian region. Jafri [1] mentioned about 23 species of Draba from Pakistan and Kashmir. In our previous studies about recent taxonomic revision of the Draba genus, we reported 30 species which include 5 new species from the area taking account the one under discussion[12,13].

The application of pollen morphology to plant systematics is

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Page 2 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

comparatively a recent trend. It has already provided a wealth of taxonomically useful information. In terms of taxonomic – phylogenetic usefulness, pollen diameter, aperture type, their number, position, structure and the internal structure of exine are the most important characters [14]. Pollen data are quite helpful in the construction of diagnosis of new species. The classification of pollen is based on number, position and character analysis known as “NPC” system, suggested by Erdtman [15]. This system helps in the formation of diagnosis below family level. The pollen characters have often been in agreement with conclusions drawn from other fields of study, particularly anatomy.

Chiguriaeva [16] was the first worker to examine the pollen morphology of the family Brassicaceae in relation to taxonomy. Later Javied and Naqshi [17] also utilized pollen data in the classification of family Brassicaceae. Jonsell [18] also examined pollen morphology of the family during monographic studies. Lahham and Al-Essawi [19] reported the pollen morphology of the family Brassicaceae from Jordan. Pollen morphology of the family Brassicaceae has been examined by various other researchers in past [15,20-22], however, the most comprehensive study of Brassicaceae pollen was carried out by Rollins and Banerjee [23]. Christian Brochmann [24] described pollen morphology of species of Nordic Draba. Though, Perveen et al. [25] reported the pollen morphological studies of the family Brassicaceae from Pakistan. After nearly half a century of research on the taxon, systematic relationship between pollen morphology and all plant morphological features was lacking. Present investigations are based on the pollen morphology of nineteen species of genus Draba of the family Brassicaceae viz. D. setosa, D. oreades, D. korschinskyi, D. cahcemirica, D. affghanica, D. olgae, D. trinervis, D. altaica, D. glomerata, D. winterbottomii, D. lasiophylla, D. lanceolata, D. tibetica, D. falconeri, D. nemorosa, D. melanopus, D. stenocarpa, D. gracillima, D. nuda were observed under light and scanning electron microscopes. The present study assisted in finding out taxonomic significance of pollen morphology in the delimitation of the genus Draba.

Materials and Methods

Plant Material

The florets of fresh & dried specimens of some species of genus Draba (Family Brassicaceae) viz., D. setosa, D. korschinskyi, D. cachemirica, D. affghanica, D. olgae, D. trinervis, D. altaica, D. glomerata, D. winterbottomii, D. lasiophylla, D. lanceolata, D. lanceolata var. sonmargensis, D. tibetica, D. falconeri, D. nemorosa, D. melanopus, D. stenocarpa, D. gracilima, D. nuda were extracted from freshly collected material from the field and herbarium specimen of Quaid-i-Azam University, Islamabad.

Light and Electron Microscopy

The pollen grains were prepared for light (LM) and scanning microscopy (SEM) by the standard methods described by Erdtman [26]. The scanning electron micrography was carried out in the Centralised Science Labs, Karachi University. Pollen diameter, polar

axis (P) and equatorial diameter (E), aperture size, apocolpium, mesocolpium and exine thickness were measured (Tables 1-3). The terminology used was obtained from previous reports [26-28].

Statistical Analysis of the Data

The data were subjected to analysis of variance using a COSTAT computer package (Cohort Software, Berkeley, California), version 6.4 and comparison among mean values of species was made by Duncan’s Multiple Range Test [29].

Results and DiscussionA summary of pollen morphological characters of the nineteen species of genus Draba is presented in Table 1 and 2. Quantitative observations are recorded under Scanning electron microscope. Whereas scanning electron micrographs of selected species of the genus are presented in Figure 1.

The pollen grains of all the species studied are similar in morphology hence the genus is stanopalynous.

Class

The class of all the pollen grains studies is tricolpate in all the species observed in this study.

Size

The size of pollen grains (polar axis × equatorial diameter) ranges from 15.52 x 17.23 - 26.29 x 18.2. D. winterbottomii was observed to be the smallest (15.5 – 16.8) and D. falconeri has the largest (18.4 - 30.57). The P/E (Polar/ Equatorial diameter) ratio varied from 119 – 171. This lowest ratio was found in D. setosa (119) and the highest in D. nemorosa (171). This range shows existence of slight variation in size among different species of the genus Draba. (Table: 2)

Symmetry and Shape

Pollen grains are radially symmetrical, isopolar, isodiametric and monads. Outline is trilobed, with apertures on the angles of the outline of the pollen grain, circular, angular, semi- angular in polar view and sub- prolate, prolate and prolate-spheroidal in equatorial view, showing great variation in pollen size. The most common shape is prolate, a type found in all species of the genus observed in the current study. Some Draba species have prolate- spheroidal or subprolate pollen grains as well. These results are congruent with the results of other researchers [19,23,25,26]. The shape of pollen grains varies very rarely within a genus.

Pollen grains of all investigated species of Draba are tricolpate [24,25]. Minor variations in aperture size were observed. The colpi are usually elongated nearly to the poles. Although exine ornamentation of the pollen grains plays a vital role within the family Brassicaceae [4,24,30], but at no significant variations occur at the species level with in a genus. Exine ornamentation remains hetero brochate reticulate with lumina equal to or exceeding the muri in size, in all species examined.

Apertures vary in length, mostly broad in centre and have acute ends. Exine sculpturing is heterobrochate reticulate with lumina

Page 3 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Figure 1: Electron micrographs of selected species of Draba L., from Pakistan, showing exine sculpturing (a), polar (b) and equatorial view (c).

Page 4 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

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Figure 2: Equitorial length of pollen grains in different species of Draba. The data represents mean of 6 replicates and all such means which share a common English letter are similar; otherwise differ significantly at P< 0.05

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Figure 3: Equitorial diameter of pollen grains in different species of Draba. The data represents mean of 6 replicates and all such means which share a common English letter are similar; otherwise differ significantly at P< 0.05

Page 5 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

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Figure 4: Polar diameter of pollen grains in different species of Draba. The data represents mean of 6 replicates and all such means which share a common English letter are similar, otherwise differ significantly at P< 0.05

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Figure 5: Colpus length of pollen grains in different species of Draba. The data represents mean of 6 replicates and all such means which share a common English letter are similar; otherwise differ significantly at P< 0.05

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Page 6 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

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Figure 6: Distance between apertures of pollen grains in different species of Draba. The data represents mean of 6 replicates and all such means which share a common English letter are similar, otherwise differ significantly at P< 0.05

Figure 7: Hierarchical Cluster Analysis of Draba L. species on the basis of palynology.

equal to or exceeding the muri in size. Colpus length varies from 10.19 - 19.73. The lowest value D. falconeri and D. nemorosa and D. stenocarpa have the highest value. Exine thickness varies from 0.75– 2.24, the lowest value observed in D. lanceolata and highest in D. gracillima.

The quantitative characters like equatorial length & diameter, P/E ratios, polar diameter, colpus length, distance between apertures, exine thickness and shape of pollen grains (coded) were analyzed by One-way ANOVA software (Table 3) and the mean values obtained were subjected to Hierarchical cluster analysis. The results revealed that the highest dissimilarity exists between D. setosa & D. nemorosa. Figures 2-6 show the graphical representation of these statistical analyses exhibiting relationships among different Draba species. Moreover, the data was found to be highly significant (Supplementary Table 1 and 2).

Hierarchical cluster analysis resulted in two main clades (Figure 7), clade I & II. Clade I includes species: D. setosa D. oreades, D. affghanica, D. trinervis, D. winterbottomii, D. tibetica, D. altaica, D. lasiophylla, D. nuda, D. glomerata. Species included in clade II are: D. falconeri & D. stenocarpa, D. lanceolata, D. melanopus, D.

gracillima, D. korschinkskyi, D. cachemirica, D. olgae & D. nemorosa. The two clades distinctly vary from each other by clade I having sub-prolate kind of pollen grains as most common along with other kinds. While, the members of clade II contain prolate kind of pollen grains predominantly. The other major dissimilarity between two clades is size of grains. Clade II consists of comparatively larger grains with greater P/E ratio & greater value of exine thickness.

The species in clade I, closely relate to each other, in their equatorial length, diameter, P/E ratios and distance between apertures. Equatorial length of these species is in range of 16 – 22.6 µm; diameter 12.9 – 17.9 µm; P/E ratio 119.6 – 142.1; polar diameter 12.5 – 17.2 µm; colpus length 10.5 – 15.9 µm; distance between apertures 7 – 10.2 µm and exine thickness 0.87 – 2.19 µm. D. glomerata seem little different from rest of the members by having prolate shaped pollen grains more numerous. Some sub- prolate pollen grains also occur in this species but it lacks prolate - spheroidal pollen grains, a character found in other members of the clade.

Similarly species falling in clade II contain: equatorial length in range of 18.4 – 26.3 µm, width 11.1 – 16.9 µm; P/E ratio 150.2 – 171.3; polar diameter 13.6 – 18.2 µm; colpus length 10.2 – 20.4 µm;

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Page 7 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

Supplementary Table 1: Data matrix of Draba L. species for Hierarchical Cluster Analysis on the basis of palynology

No Taxon Equi length um Equidiam P/ E ratio Pol diam Col leng dis btap Ex thick Pl Shp

1 D. setosa 21.3 17.9 119.4 17.2 13.7 7 1.67 4

2 D. oreades 19.9 16.2 122.3 15.5 10.7 8.8 1.07 2

3 D. korschinskyi 20.7 14.05 150.2 13.9 15.2 8.1 1 3

4 D. cachemirica 25.5 14.9 171.1 14.8 18.7 9.8 2.19 1

5 D. affghanica 20.9 17.5 119.8 16 12 7.8 1.95 4

6 D. olgae 22 13.9 163.8 14.3 19.3 8.4 2.14 3

7 D. trinervis 16 13.2 123.4 15.8 10.9 10.1 0.87 4

8 D. altaica 18.6 14.03 132.3 14.6 11.9 8.2 1.94 2

9 D. glomerata 18.3 12.9 142.1 15 13.5 9.3 1.37 2

10 D. winterbottomii 15.5 12.9 119.6 12.5 10.5 8.1 1.1 4

11 D. lasiophylla 19.4 14.1 136.7 12.5 12.7 8.2 0.93 3

12 D. lanceolata 21.4 13.8 159.4 15.5 14.8 10.3 0.75 3

13 D. tibetica 19.4 15.3 127.3 15.9 13.9 10.2 1.96 3

14 D. falconeri 26.3 16.9 155.4 16.9 20.4 11.6 2.07 2

15 D. nemorosa 18.4 11.1 171.3 13.6 10.2 7.2 1.86 1

16 D. melanopus 20.5 13.1 158.4 16.3 15.7 10.6 2.22 1

17 D. stenocarpa 24.1 15.3 159.1 15.8 19.7 9.6 2.01 2

18 D. gracillima 24.8 15.9 156 18.2 12.8 10.6 2.24 2

19 D. nuda 22.6 16.4 138.2 15 15.4 8.5 2.19 3

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Page 8 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

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BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Page 9 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

distance between apertures 7.2 – 11.6 µm and exine thickness 0.75 – 2.24 µm. D. nemorosa shows more differences with rest of the group members by having only prolate type of grains along with relatively smaller size.

ConclusionIn present study stenopalynous nature of genus Draba is confirmed

as no major variations were seen among the species studied. Minute variations do exist which are reflected in the dendrogram by following into two distinct groups. Where as degree of similarity in palynological characters is same as observed in other taxonomic traits. No Significant deviation from systematic relationship among all morphological and pollen morphology were observed. Hence we can say that palynological traits can also be considered while

Table 3: Statistical analysis of quantitative characters of poeeln grains of genus Draba L.

Quntitative Characters Source df Type I SS MS F value P value

1 Equatorial length of pollen grains

Species 18 1567.74 87.09 20.37 0.000***

Error 171 731.09 4.27 <

Total 189 2298.84

Model 18 1567.74 87.09 20.37 0.000***

2 Equitorial diameter of pollen grains

Species 18 583.81 32.43 12.57 0.000***

Error 171 441.1 2.57 <

Total 189 1024.92

Model 18 583.81 32.43 12.57 0.000***

3 P/ E ratio

Species 18 60830 3379.4 10.47 0.000***

Error 171 55194.1 322.77 <

Total 189 116024.1

Model 18 60830 3379.4 10.47 0.000***

4 Polar diameter of pollen grains

Species 18 394.9 21.94 13.07 0.000***

Error 171 286.92 1.68 <

Total 189 681.82

Model 18 394.9 21.94 13.07 0.000***

5 Colpus length

Species 18 1883.9 104.65 9.65 0.000***

Error 171 1852.9 10.83 <

Total 189 3736.8

Model 18 1883.9 104.65 9.65 0.000***

6 Distance between apertures

Species 18 302.61 16.81 4.98 0.000***

Error 171 577.04 3.37 <

Total 189 879.65

Model 18 302.61 16.81 4.98 0.000***

7 Exine thickness

Species 18 51.94 2.88 26.96 0.000***

Error 171 18.3 0.107

Total 189 70.24

Model 18 51.94 2.88 26.96 0.000***

BAOJ Biotech, an open access journal Volume 2; Issue 1; 009

Page 10 of 10Citation: Kaleem Ullah Kakar, Raqeeb Ullah, Zarqa Nawaz, Muhammad Ishtiaq, Faizan Ullah, et al. (2016) Palynological Studies of Genus Draba L. (Brassicaceae) From Pakistan. BAOJ Biotech 2: 009.

classifying taxa. These palynological characters can provide an additional support for the delimitation of a taxon.

AcknowledgementWe are thankful to curator and staff of Herbarium Quaid-i- Azam University, Islamabad for provision of the necessary plant material and related facilities for the study.

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