Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020) © The Egyptian Society of Experimental Biology DOI: 10.5455/egyjebb.20201112065657 AARU Impact Factor: 1.3

RESEARCH ARTICLE

Eman A. Karakish Suad Al-Ruzayza Kadry Abdel Khalik

Comparative anatomical studies of some species of family from Saudi Arabia and its systematic significance

ABSTRACT: In this study, the micromorphological INTRODUCTION: characters of 17 species belonging to seven The Malvaceae is a cosmopolitan family, genera of family Malvaceae, collected from concentrated in the tropical and subtropical different localities in Saudi Arabia were region. It comprises ≈244 genera and over examined. These characters used in analysing 4225 species (Hutchinson, 1967, Fryxell, the relationship among the studied species 1988, La Duke and Doebley, 1995, viz., outline of stem, petiole and lamina in Christenhusz and Byng, 2016). Collenette cross section, trichomes, crystals, ducts, star- (1985) represented Malvaceae by 24 species shape idioblasts, aspects of secondary under 10 genera in Saudi Arabia, while growth. The anatomical features are used for Chaudhary (1999) recorded 31 species the construction of an artificial key. belonging to 17 genera. Depending on the presence of trichomes, the Systematic anatomy has a long history studied species separate in two main groups; since the invention of the microscope. first group contain the species of Althaea, Anatomy as well as morphology considered as Hibiscus and Malva (owing to the stem the bone skeleton of taxonomy to study vascular system), second group contain the the phylogeny and evolution (Endress et al., four remaining genera where their 2000). classification depend on many attributes such A number of anatomical studies were as, cross section of stem, petiole and leaf, performed on Malvaceae from various arrangement of trichomes, and ducts. aspects. The epidermal anatomy has been described in the leaves of some Malvaceae KEY WORDS: species (Inamdar and Chohan, 1969; Rao and Malvaceae, Anatomy, Leaf, Petiole, Stem. Ramayya, 1977; Celka et al., 2006; Shaheen et al., 2010). Previous studies have shown that stem and leaf micromorphology can be CORRESPONDENCE: used to distinguish genera and species in order (Inamdar et al., 1983; Yu-Long Eman A. Karakish and Yan-Sheng, 1984; Hussin and Sani, Botany Department, Faculty of Science, Ain 1998; Salma, 1999 & 2000; Nurul-Aini et al., Shams University, Cairo, Egypt 2013). Jansen et al. (1998) showed that E-mail: [email protected] vascular anatomy is useful to delimit the core Malvales from other families. Chung (2002) cleared that the glandular Trichomes of 32 Suad Al-Ruzayza 1 Microcos species (Malvaceae) are very Kadry Abdel Khalik 1 & 2 important in species identification and authentication. Olotuah (2014) studied the 1-Biology Department, Faculty of Applied anatomy of the leaf epidermis and petiole of Science, Umm-Al-Qura University, two selected species of Hibiscus to show the Mecca, Saudi Arabia difference between them. Naskar (2016) 2-Botany and Microbiology Department, studied the anatomical features in the family Faculty of Science, Sohag University, Malvaceae and construct an identification key Sohag, Egypt for the genera delimitation. Bayer and Kubitzhi (2003) classified Family Malvaceae according to the plant, flower and fruit morphology into four main tribes: 1) Kydieae. 2) Gyosspieae. 3) ARTICLE CODE:19.02.20 (including Fioria, Hibiscus, Pavonia and ). 4) Malveae including Abutilon

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204 Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020) alliance (Abutilon) and Malva alliance (Altheae and Malva). MATERIAL AND METHODS: The main objectives of this study are to In the present study, 17 species provide a detailed description of the belonging to seven genera of family micromorphology of the studied species of Malvaceae, subfamily Malvoideae (Bayer and Malvaceae, and to clear how far that Kubitzki, 2003) were collected from different micromorphological characters can serve in localities in Saudi Arabia. Table 1 represents taxa delimitation of the family and evaluate the list of the studied species, their tribes the usefulness of these characters in according to Bayer and Kubitzki (2003), contribution to further revision and localities and date of collection. The collected classification of this family. specimens identified according to Collenette (1985), Migahid (1989), and Chaudhary (1999). Table 1. List of the studied species, their tribes, localities and date of collection.

Date of Genus No. Species Tribe Localities collection

Abutilon bidentatum Hochst. ex Wadii Thalolah near AL-Baha, Jabal 1 18\04\2019 A.Rich. Shada, RAWRC and KSU 2 Abutilon fruticosum Guill. & Perr. Fifa mountain, Absiaa and KSU 15\04\2018 3 Abutilon grandifolium (Willd.) Sweet Fifa mountain, Alaridah and KSU. 15\02\2019 Mahil Aseir, Al_Mkwah, Wadii Al- 4 Abutilon hirtum (Lam.) Sweet. 10\01\2018 Rahjania, KSU and RAWRC

Abutilon 5 Abutilon muticum (Del.exDC.) Sweet. Malveae Alardah, Wadii beash, Adharb and KSU. 29\01\2018 Mill. Wadii Adahawat, Wadii Qusaii, Al-Edabi, 6 Abutilon pannosum (G.Forst.)Schltdl. Wadii Beash, Sabia, Mahil Aseir, Qudaid, 15\03\2018 Raidah and KSU. Wadii Qusai, Umm Al-Quraa University 7 Abutilon figarianum Webb. 10\03\2018 and KSU. Abutilon ramosum (Cav.) Guill. & Shada mountiain, Al-Baha road, Al- 8 21\04\2018 Perr. Mkwah and KSU. Shaqraa, Ramah, Qassim Road and Althea L. 9 Althaea ludwigii L. Malveae 19\01\2019 RAWRC.

10 Hibiscus deflersii Schweinf. ex Cufod. Wadii Al- sheaf,Taif. 19\05\2019 Hibiscus L. Hibisceae 11 Hibiscus micranthus L.f. Raidah and Jabalah Mountain. 12\03\2018 Ushaqur, Al_Qasim- Buradah, AL-Jubail 12 Malva neglecta Wallr. 04\04\2019 and Rawdah kharaim. Malva L. 13 Malva parviflora L. Malveae Alkarj and Jabalah Mountain. 03\05\2019 Al-Sawdah, AL-ahsaa and Jabalah 14 Malva verticillata L. 03\04\2018 Mountain. Pavonia arabica Hochst. & Steud. Ex Pavonia Cav. 15 Hibisceae Bani Malik and RAWRC. 05\04\2019 Boiss. Senra Cav. 16 Senra incana Cav. Hibisceae Harrat Al-Shara. 21\01\2019 Fioria Mattei 17 Fioria dictyocarpa (Webb) Mattei Hibisceae AD darb near Abha and KSU. 05\02\2018

The species under investigation were then double stained using safranine and light matched against photos of authentic green combination and mounted in Canada specimens in the herbaria of KSU (King Saud Balsam according to method of Johanson University), RAWRC (National Research (1940). The sections were examined using centre of Agriculture and Livestock, Riyadh, OPTIKA B-150 light microscope and the Ministry of agriculture) and UQU (Umm Al - photos were taken using Nikon Coolpix p600 Qura University). The collected species were Digital Camera, the magnification power was pressed and prepared as herbarium expressed by (X). specimens, deposited in the Herbarium of Biology Department, Faculty of Applied RESULTS AND DISCUSSION: Science, and Umm Al-Qura University. The obtained anatomical characters of The shoot system of the studied the species under investigation were species was preserved in 70% alcohol. Cross summarized as follows (Table 2, Figs 1-17). section of the stem, petiole and lamina were made using hand microtome at 14 - 18 µm., ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

Karakish et al., Anatomical studies of some species of family Malvaceae from Saudi Arabia and its systematic significance 205

Table 2. the Micromorphological Characters of the species under study belonging to family Malvaceae Plant species 1 2 3 4 5 6 7 8 organ characters

Cross section I- terete ± terete I- terete ± terete I- terete terete terete ±terete

Shape ± cubic ± cubic ± cubic TE ± cubic ± cubic ±cubic cubic ± Epidermis Out wall straight straight straight straight straight straight papillose papillose Cuticle thin thin thick thin thin thin thick thin

Distribution DS DS MS DS LS DS DS DS Trichomes Types MU & MM MU, MBM MU, MBM MBM MU, MBM MU, MBM MU, MBM MBM

Types ------Ducts

Location ------

druses & Types druses druses druses druses druses druses druses

stem solitary Crystals cortex, cortex, cortex, cortex, cortex, cortex & cortex & cortex & Location phloem & phloem & phloem & phloem & phloem & pith phloem pith pith pith pith pith pith Thickness ±wide ±narrow narrow ±wide ±narrow narrow narrow narrow AC 3-4 Ch 1-2 Ch 1-2 Ch 1-2 Ch 1-2 Cortex Ch 1-2 rows, rows, P, CF 2-3 rows, rows, Types of cells rows, P, PF rows, P, P 4-5 rows P 4-5 rows P 4-5 P 3-4 P 3-4 rows PF rows, CF rows, PF rows, PF Type of vascular bundles CR CR CR CR PR CR CR CR narrowly narrowly narrowly narrowly narrowly narrowly narrowly 2ry interfascicular xylem -- fiber cells fiber cells fiber cells fiber cells fiber cells fiber cells fiber cells Thickness ±wide wide wide ±wide wide wide wide wide Pith Types of cells P P AC P P AC AC P concave- plain- sulcate- ±plain- Cross section ovate ± terete terete ± terete convex convex convex convex Shape cubic cubic cubic RE ±cubic RE cubic ±cubic Epidermis Cuticle thin thin thin thin thin thin thin thin

Distribution MS DS DS MS LS DS DS DS

Trichomes

Types MU, MBM MU, MBM MU, MBM MBM MU, MBM MU, MBM MU, MBM MBM petiole druses & druses Crystals druses druses druses druses druses druses solitary (DS) 4 main & 4 main, 4 Vascular bundles No. 4- 6 4 4- 6 4 4 7-8 2 small small lateral AC 4-5 Ground tissue P P P P, AC P P P rows, P Shape ±cubic cubic cubic TE cubic cubic cubic TE Epidermis Cuticle thin thin thin thin thin thin thin thin

Distribution MS DS MS DS LS DS DS DS Trichomes MU & Types MBM UU, MM MBM MBM MU, MBM MU, MBM MBM

MBM

Crystals + + + + + + +(DS) +

Lamina PP 2 PP 2 PP 2 PP 2 PP 2 PP 2 layers, layers, layers, layers, layers, layers, Mesophyll ST 3-5 Ch Ch ST 3 ST 2-3 ST 2-3 ST 3 ST 3 layers layers layers layers layers layers Idioblasts -- + + ------obtuse- obtuse- obtuse- ±flat- obtuse- obtuse- obtuse- obtuse- Shape of midrib convex convex convex convex convex convex convex convex Midrib cells P P P P P P Ch, P P

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206 Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020)

Cont. Table 2. Plant species 9 10 11 12 13 14 15 16 17 organ characters Cross section ± terete terete terete I- ovate I- terete I- terete terete ±terete ovate Shape cubic ±RE ±RE ±cubic ±cubic ±cubic RE ±TE ±TE ± Epidermis Out wall ± straight straight ±straight ±straight ±straight straight ±straight ±straight papillose Cuticle thin ±thick thin thin thin thin thick thin thin Distribution -- -- LS ------LS MS MS Trichomes MU, UU, Types -- -- MU, MB ------UU, MBM BU, MBM MBM Types -- + + ------+ -- -- Ducts cortex & cortex & Location -- cortex ------pith pith druses & druses & Types -- druses ------druses druses

solitary solitary

cortex, Crystals beneath stem phloem & cortex, Ac, near cortex & cortex Location -- pith, ------phloem & bundles pith &pith solitary in pith in pith pith Thickness narrow ±wide narrow ±narrow ±narrow ±narrow wide ±narrow narrow Ch 2-3 Ch 2 SP 5-7 Ch 3 Ch 2-3 Cortex rows, rows, Ch 2-3 Ch 2-3 Ch 2-3 rows, P 3- Ch 1-2 rows, Types of cells rows, P 4- P wide P 2-3 rows, P rows, P rows, P 5 rows, rows, P P 3-4 5 rows region rows, PF PF rows Type of vascular bundles CR CR CR 8-10 PVB 8-10 PVB 8-10 PVB CR CR CR narrowly widely xylem narrowly narrowly fiber 2ry interfascicular xylem fiber fiber ------vessels & fiber fiber cells cells cells xylem fiber cells cells Thickness wide ±wide ±narrow wide wide wide ±narrow ±wide wide Pith Types of cells P P AC P P P P P P flat- sulcate- sulcate- flat- plain- Cross section ±terete I- ovate ±terete ±terete convex convex convex convex convex Shape cubic ±RE ±RE RE cubic cubic ±RE ±cubic ±cubic Epidermis Cuticle thin ±thick ±thick thin thin thin thick thin thin Distribution ------LS LS ±DS Trichomes MU, UU, Types ------UU, MBM BU, MBM MBM

petiole druses Crystals -- druses ------druses (DS) 4 main & Vascular bundles No. 4 4 CR 4 7-9 6 4 4 2 small lateral Ch 2-3 PP1-2 Ch 1-2 Ch 1-2 Ch 1-2 AC 2-3 AC 2-3 Ch 1row, Ground tissue P, AC rows, P rows, P rows, P rows, P rows, P rows, P rows, P P Shape TE TE cubic ±cubic TE TE cubic cubic TE Epidermis Cuticle thin thin thin thin thin thin thin thin thick Distribution ------LS LS LS Trichomes MU, UU, Types ------UU, MBM UU, MBM MBM

Crystals -- + + + + -- -- + + PP 2 PP 2 PP 1-2 PP 1-2 PP 2 PP 2 PP 2 layers, layers, layers, layers, layers, PP 3-4 layers, Lamina Mesophyll PP layers, ST ST 3 ST 2-3 ST 2-3 ST 2-3 ST 2-3 rows ST 3 3-4 layers layers layers layers layers layers layers Idioblasts -- + + ------+ flat- obtuse- obtuse- flat- obtuse- flat- flat- obtuse- obtuse- Shape of midrib convex convex convex convex convex convex convex convex convex Midrib cells P P P P P P P P P Absent= --, Angular collenchyma=AC, Bi-cellular Uniserriate = BU, Chlorenchyma= Ch, Complete rings of fibers= CF, Complete ring of primary vascular bundles= PR, Complete ring of secondary tissues = CR, Densely scattered= DS, Irregular = I, Loosely scattered= LS, Moderately scattered= MS, Multicellular uniseriate = MU, Palisade parenchyma= PP, Patches of fibers or sclerenchyma=PF, Polyhedral parenchyma= P, Present=+, Primary vascular bundles= PVB, Radially elongate = RE, Sclerenchyma = S, Spongy tissue= ST, Stellate with bicellular foot= MB, Stellate with bi-multicellular foot= MBM, Stellate with multicellular foot= MM, Subepidermal periderm= SP, Tangentially elongated= TE, Unicellular uniserriate= UU.

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Fig. 1. Micromorphology of Abutilon bidentatum. A&B, T.S. of the stem (X = 4, X = 40, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

Fig. 2. Micromorphology of Abutilon fruticosum. A, T.S. of the stem (X=4). B, T.S. of the petiole (X = 4). C & D, T.S. of the lamina (X = 10, X = 40, respectively).

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208 Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020)

Fig. 3. Micromorphology of Abutilon grandifolium. A, T.S. of the stem (X = 4). B, T.S. of the petiole (X = 4). C & D, T.S of the lamina (X = 4, X = 10, respectively).

Fig. 4. Micromorphology of Abutilon hirtum. A, T.S. of the stem (X=4). B, T.S. of the petiole (X = 4). C & D, T.S of the lamina (X = 10, X = 40, respectively).

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Fig. 5. Micromorphology of Abutilon maticum. A & B, T.S. of the stem (X = 4, X = 40, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

Fig. 6. Micromorphology of Abutilon Pannosum. A & B, T.S. of the stem (X = 4, X = 40, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

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210 Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020)

Fig. 7. Micromorphology of Abutilon fgarianum. A, T.S. of the stem (X = 4). B & C, T.S. of the petiole (X = 4, X = 40, respectively). D, T.S of the lamina (X = 10).

Fig. 8. Micromorphology of Abutilon ramosum. A & B, T.S. of the stem (X = 4, X = 10, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 4).

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Fig. 9. Micromorphology of Althaea ludwigii. A & B, T.S. of the stem (X = 4, X = 10, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

Fig. 10. Micromorphology of Hibiscus delfersii. A & B, T.S. of the stem (X = 4, X = 10, respectively). C, T.S. of the petiole (X = 10). D, T.S of the lamina (X = 10).

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Fig. 11. Micromorphology of Hibiscus micranthus. A, T.S. of the stem (X = 4). B, T.S. of the petiole (X = 10). C & D, T.S of the lamina (X = 10, X = 40, respectively).

Fig. 12. Micromorphology of Malva neglecta. A, T.S. of the stem (X = 4). B, T.S. of the petiole (X = 10). C, T.S of the lamina (X = 10).

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Fig. 13. Micromorphology of Malva parviflora. A & B, T.S. of the stem (X = 4, X = 10, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

Fig. 14. Micromorphology of Malva verticillata. A, T.S. of the stem (X = 4). B, T.S. of the petiole (X=4). C, T.S of the lamina (X = 10). ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

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Fig. 15. Micromorphology of Pavonia Arabica. A & B, T.S. of the stem (X = 4, X = 40, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10).

Fig. 16. Micromorphology of Senra incana. A, T.S. of the stem (X = 4). B, T.S. of the petiole (X = 4). C, T.S of the lamina (X = 10).

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Fig. 17. Micromorphology of Fioria dictyocarpa. A & B, T.S. of the stem (X = 4, X = 10, respectively). C, T.S. of the petiole (X = 4). D, T.S of the lamina (X = 10). Stem anatomical characters: b. Types: stellate trichomes present in 1. Outline: the 12 species. These species have stellate type with bicellular foot in Hibiscus Terete in five species, irregularly to ± micranthus, multicellular foot in Abutilon terete in ten species; while irregularly ovate bidentatum and bi- multicellular foot in ten to ovate in Malva neglecta and Fioria species. Multicellular uniseriate present in dictyocarpa. eight species, unicellular uniseriate in 2. Epidermis: Pavonia arabica and Senra incana, bicellular a. Shape: ±cubic in nine species, cubic uniseriate in Fioria dictyocarpa. in two species, tangentially elongated in three In this study, the author regarded that species (Abutilon hirtum, Senra incana and Abutilon hirtum and Abutilon ramosum contain Fioria dictyocarpa) and radially elongated in one type of trichome (stellate with bi- three species (the two studied species of multicellular foot which are densely genus Hibiscus and Pavonia arabica) distributed), two types of trichomes present in b. Outer wall: either ±straight to straight nine species (multicellular uniseriate and in 14 species or ±papillose to papillose in the stellate with bi- multicellular foot in five remaining three species (Abutilon species, multicellular uniseriate and stellate grandifolium, Abutilon ramosum and Hibiscus with multicellular foot in Abutilon bidentatum, micranthus). multicellular uniseriate and stellate with c. Cuticle: either thin in 13 species or multicellular foot in Hibiscus micranthus, thick in the remaining four species. unicellular uniseriate and stellate with bi- multicellular foot in Pavonia arabica, bicellular 3. Trichomes: uniseriate and stellate with bi- multicellular Present in 12 species while absent in foot in Fioria dictyocarpa). Senra incana have the five remaining species (Althea ludwigii, three types of trichomes (multicellular Hibiscus deflersii and the three studied uniseriate, unicellular uniseriate and stellate species of Malva). with bi- multicellular foot). a. Distribution: densely scattered in six 4. Ducts: species, moderately scattered in three Absent in 14 species, present in the species and loosely scattered in three cortex and pith of Hibiscus deflersii and species. Pavonia arabica while present only in the cortex of Hibiscus micranthus. ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

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5. Crystals: b. Cuticle: thin in 14 species, and thick Druses only present in ten species in the two studied species of Hibiscus and (regarded in cortex, phloem and pith of seven Pavonia Arabica. species, in cortex and pith of three species 3. Trichomes: and in cortex and phloem of Abutilon Present in 11 species while absent in pannosum), druses and solitary in Abutilon the six remaining species (Althea ludwigii, two bidentatum, Hibiscus deflersii and Fioria studied species of Hibiscus and the three dictycarpa, while crystals absent in Althea studied species of Malva). ludwigii and the three studied species of a. Distribution: densely scattered in six genus Malva. species, moderately scattered in two species 6. Cortex: and loosely scattered in three species. a. Width: the cortex wide in four b. Types: stellate trichomes with bi- species, while ±narrow to narrow in the multicellular foot present in the studied 11 remaining 13 studied species. species. Two types of trichomes present in six b. Types of tissue: in 13 species of the species (multicellular uniseriate and stellate studied species the outer layer of cortex with bi- multicellular foot). Trichomes of consists of chlorenchyma cells (chlorenchyma unicellular uniseriate and stellate with bi- consists of two- three rows in seven species multicellular foot present in Pavonia Arabica, and two-three rows in six species); followed while bicellular uniseriate and stellate with bi - by numerous rows of parenchyma only in ni ne multicellular foot in Fioria dictyocarpa. Senra species while the parenchyma followed by incana have three types of trichomes patches of fibres in four species. In Abutilon (multicellular uniseriate, unicellular uniseriate grandifolim and Abutilon figarianum, the outer and stellate with bi- multicellular foot). layer of cortex consists of numerous rows of 4. Crystals: parenchyma cells ended by ±complete ring or Druses present in ten species where it patches of fibres respectively. In Abutilon densely scattered in Abutilon figarianum and fruticosum, the cortex consists of three- four Fioria dictyocarpa. Druses and solitary, rows of angular collenchyma followed by four- present in Abutilon bidentatum. Crystals five rows of parenchyma and ended by absent in the remaining six species. complete ring of fibres. Pavonia arabica, the only species in our studied that have five- 5. Vascular bundles number: seven rows of subepidermal periderm followed Four separated vascular bundles by three- five rows of parenchyma ended by present in eight species. Six bundles present patches of fibres. in Malva verticillata. Four- six ±equal vascular 7. The vascular system: bundles present in Abutilon bidentatum and A. grandifolium. Seven- nine ± equal vascular In the form of complete or continuous bundles present in Abutilon Pannosum and normal siphonostelic in 13 species. Primary Malva parviflora. There are four main bundles separated collateral vascular bundles rang and two small ones in Abutilon ramosum and from eight- ten present in the three studied Fioria dictyocarpa, while there are four main species of Malva. In Abutilon muticum the bundles and four small ones in Abutilon vascular tissue system consists of complete figarianum. In Hibiscus micranthus there is ring of primary growth. complete ring of secondary vascular tissue 8. Pith: system a. Width: wide in 15 species while 6. Ground tissue: narrow in Hibiscus micranthus and Pavonia Polyhedral parenchyma only present in Arabica. six species, one- three rows of chlorenchyma b. Types of cells: polyhedral followed by parenchyma cells present in five parenchyma in 13 species and angular species, two- five rows of angular collenchyma in Abutilon grandifolium, A. collenchyma followed by parenchyma present pannosum, A. figarianum and Hibiscus in three species, polyhedral parenchyma micranthus followed by angular collenchyma in the centre Petiole anatomical characters: in two species. Palisade parenchyma followed 1. Outline: by parenchyma present only in Hibiscus deflersii. ± terete to terete in six species, irregular ovate to ovate in two species, plai n- Lamina anatomical characters: convex in three species, sulcate-convex in 1. Epidermis: three species, flat-convex in two species and a. Cell Shape: cubic in ten species, concave-convex in Abutilon grandifolium. while tangentially elongated in eight species. 2. Epidermis: b. Cuticle: except Fioria dictyocarpa a. Cell Shape: ±cubic to cubic in 11 with thick cuticle, the remaining 16 taxa have species, while radially elongated in the thin cuticle. remaining six species. ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

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2. Trichomes: trichomes in characterizing Malvales. The Present in 11 species while absent in previous study disagrees with Munir et al. the six remaining species (Althea ludwigii, two (2011), Akbar et al. (2014) and Olotuah studied species of Hibiscus and the three (2014), their results were that Malva studied species of Malva). parviflora has different type of trichomes. We agree with Munir et al. (2011) and Akbar et al. a. Distribution: densely scattered in five (2014) who regarded the absence of duct in species, moderately scattered in two species Malva parviflora. and loosely scattered in four species. Our previous observations are accord b. Types: stellate trichomes with bi- with Amos (1951), who discussed the multicellular foot only present in four species. importance of crystals in taxonomy as Two types of trichomes present in three diagnostic tools, he mentioned that, their species (multicellular uniseriate and stellate mode of distribution is important in taxonomy. with bi- multicellular foot). Trichomes of The observations disagree with Mazen (2004) unicellular uniseriate, and stellate with bi- and Faheed et al. (2012) in their results of the multicellular foot present in Pavonia arabica presence of crystals in Malva parviflora. and Fioria dictyocarpa, while unicellular uniseriate, and stellate with multicellular foot The present results agree with El- in Abutilon fruticosum. Senra incana have the Shazly (2013) in the composition of the cortex three types of trichomes (multicellular and separation of vascular bundles in Malva uniseriate, unicellular uniseriate and stellate parviflora stem with bi- multicellular foot). The results agree with the finding of 3. Crystals: Öznur and Tuğba (2006) and Nurul-Aini et al. (2013) on Malva neglecta and some species Druses present in 14 species while of Malvaceae (Grewioideae), respectively, absent in the remaining three species. who stated that some petiolar anatomical 4. Mesophyll: characters viz. outline, vasculature and Dorsiventral in 13 species, while trichomes are useful and of taxonomic value isobilateral in four species; the mesophyll in species delimitation. consists of chlorenchyma in Abutilon Epidermal cells of the leaf and fruticosum and Abutilon figarianum, while it is trichomes are useful anatomical tools (Munir palisade parenchyma in Althaea ludwigii and et al., 2011). Olotuah (2014) used the Pavonia Arabica. distribution and quality of the druses crystals 5. Idioblasts: on the leaf epidermal cells of two species of Absent in 12 species and present in five Hibiscus, we agree with his results, while species. disagree with the presence of trichomes. 6. Shape of midrib: Our finding in the present study agree with Shaheen et al. (2009) and Gomaa et al. Obtuse- convex in 12 species, and flat- (2016) in their results on genus Abutilon Mill convex in the remaining five species. which have similar characters such as 7. Midrib cells: different type of trichomes and calcium Except Abutilon figarianum which have oxalate crystals present in cortex, phloem and chloernchyma and polyhedral parenchyma pith of stem. Said et al. (2018) have similar cells, all the remaining 16 species have characters in studying Malva species such as polyhedral parenchyma only. absence of trichomes, the composition of cortex, crystals, and the vascular tissue Anatomical features are widely used in system in the stem. systematic for identification, classification and for indicating patterns for relationship that The anatomical characters of the may have been obscured by superficial studied species are varied considerably. So, convergence in anatomical features and these characters are useful to delimit the morphology (Essiett, 2004). Watson and species. Dallwitz (1992) gave information about the An artificial identification key to the general anatomical characteristics of the species is given below considering the studies family Malvaceae. anatomical features. Our previous results confirm with (1) Presence of trichomes on the stem, petiole Ramaya and Rao (1976), Inamdar et al. and lamina………………..……….……. (2) (1983) and Dorr (1990) who reported that (1) Absence of trichomes on the stem, petiole epidermal layer in Malvaceae characterized and lamina……………………...…...…. (12) by presence of various types of hairs which are broadly regarded as useful for (2) Presence of ducts in cortex and pith of establishing the systematic relationships stem, with narrow stem pith, within the family Malvaceae. Such view was mesophyll consists of palisade also submitted buy Bayer and Kubitkzi (2003) parenchyma only……...…….. Pavonia arabica that used the character of the eglandular ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

218 Egypt. J. Exp. Biol. (Bot.), 16(2): 203 - 221 (2020)

(2) Absence of ducts, wide stem pith, trichomes moderately arranged on petiole and mesophyll consist of palisade and spongy leaf …. …………….…… Abutilon bidentatum tissue or chlorenchyma (9) Absence of solitary crystals in stem and only………………………………………..…….. (3) petiole, presence of fibre cells in the cortex, (3) Stem cross section ovate, presence of narrow pith, petiole cross section terete or bicellular uniseriate trichome on stem and sulcate- convex, trichomes densely arranged petiole, petiole ground tissue consists of one on petiole and leaf ……………….….……... (10) row of collenchyma followed by parenchyma (10) Presence of chlorenchyma followed by cells …………………….… Fioria dictyocarpa parenchyma and ended with fibres in stem (3) Stem cross section ±terete to terete, cortex, absence of crystals in the stem pith, absence of bicellular uniseriate trichome, petiolar epidermis radially elongated, petiole petiole ground tissue consists of angular contain seven- eight vascular bundles, collenchyma and parenchyma or parenchyma mesophyll dorsiventral .. Abutilon Pannosum only ……………………………………….……. (4) (10) Absence of chlorenchyma in stem cortex, (4) Loosely arranged trichomes on petioles presence of crystals in the stem pith, petiolar and lamina, stem cortex consist of one- two epidermis cubic, petiole contain four or four rows of chlorenchyma followed by two- four main and four small vascular bundles, rows of parenchyma, absence of cortex fibres mesophyll isobilateral (chlorenchyma cells) ……………………………………………….…… (5) ……………………………………………….…. (11) (4) Densely or moderately arranged trichomes (11) Petiolar cross section terete, petiole on petioles and lamina, stem cortex consist of contain four vascular bundles, presence of one- two rows of chlorenchyma followed by idioblasts in leaves, absence of chlorenchyma four- five rows of parenchyma only or ended in the midrib ……………. Abutilon fruticosum by ± complete ring or patches of fibres (11) Petiolar cross section sulcate- convex, ……………………………………...…...………. (6) petiole contain four main and four small (5) Epidermal cells cubic in stem, primary vascular bundles, absence of idioblasts in vascular tissue system, Petiolar ground tissue leaves, presence of chlorenchyma in the consist of parenchyma midrib….………..……… Abutilon Figarianum only……………..Abutilon muticum (12) Stem contain primary vascular tissue (5) Epidermal cells tangentially elongated in system only (eight- ten separated collateral stem, secondary vascular tissue system, vascular bundles) …………………..………. (13) petiolar ground tissue consist of angular (12) Stem contain complete ring of secondary collenchyma followed by vascular tissue system ……………..……… (15) parenchyma…………...... ….. Senra incana (13) Petiolar cross section irregularly ovate, (6) Presence of multicellular uniseriate petiolar epidermis radially elongated, petiole trichomes on stem and petiole, Petiole cross contain four vascular bundles, lamina section rather than plain- convex, lamina epidermis cubic……………..… Malva neglecta epidermis tangentially elongated …………...(8) (13) Petiolar cross section terete or sulcate- (6) Absence of multicellular uniseriate convex, petiolar epidermis cubic, petiole trichomes on stem and petiole, petiole cross contain six or seven- nine vascular bundles, section plain- convex, lamina epidermis ± lamina epidermis tangentially cubic to cubic ……………………..………….. (7) elongated……………………………………… (14) (7) Outer wall of leaf epidermis straight, (14) Petiolar cross section terete, petiole petiolar epidermis radially elongated, petiolar contains seven- nine vascular bundles, lamina vascular system consists of four bundles, leaf midrib obtuse- convex ± flat- convex …………….... Abutilon hirtum ………………………….……… Malva parviflora (7) Outer wall of leaf epidermis papillose, (14) Petiolar cross section sulcate- convex, petiolar epidermis ± cubic, petiolar vascular petiole contain six vascular bundles, lamina system consists of four main and two small midrib flat- convex ………… Malva verticillata bundles, leaf obtuse- convex (15) Epidermal cells cubic in stem and petiole, ……………………...……… Abutilon ramosum absence of ducts and crystals in stem, petiole (8) Outer wall of leaf epidermis ± papillose, flat- convex in cross section, absence of trichomes moderately arranged on stem, cross idioblasts in leaves, mesophyll isobilateral, section of petiole concave- convex lamina midrib flat- …………………………. Abutilon grandifolium convex...... Althaea ludwigii (8) Outer wall of leaf epidermis straight, (15) Epidermal cells radially elongated in trichomes densely arranged on stem, cross stem and petiole, presence of ducts and section of petiole have different shape rather crystals in stem, petiole sulcate- convex or than concave- convex…………………...…...(9) terete in cross section, presence of idioblasts (9) Presence of solitary crystals in stem and in leaves, mesophyll dorsiventral, lamina petiole, absence of fibre cells in the cortex, midrib obtuse- convex…………..……………(16) wide pith, petiole cross section ovate, ISSN: 1687-7497 Online ISSN: 2090 - 0503 https://www.ejmanager.com/my/ejeb

Karakish et al., Anatomical studies of some species of family Malvaceae from Saudi Arabia and its systematic significance 219

(16) Out wall of the stem epidermal cells tissues of petiole and absence of idioblasts). straight, absence of fibre cells in the cortex, Also support the gathering of Abutilon under petiole sulcate- convex in cross section, subtribe Abutilinae (Kearney, 1951) due to the contain four vascular presence of different types of trichomes all bundles……..………………. Hibiscus delfersii over the and presence of crystals in (16) Out wall of the stem epidermal cells both stem and petiole. We agree with Kundu papillose, presence of fibre cells in the cortex, and Biswas (1947) that Fioria distinct from petiole ± terete in cross section, contain Hibiscus by the ovate stem in cross section, complete ring of secondary tissue system tangentially elongated epidermal cells, …………………………… Hibiscus micranthus absence of ducts and presence of different types of trichomes all over the plant. Kearney (1951) divided family Malvaceae into four tribes: 1) Malpeae. 2) According to Bayer and Kubitzhi (2003), Ureneae (including Pavonia). 3)Hibisceae they discussed tribe Hibisceae including (including Hibiscus). 4) Malveae; divided into Fioria, Hibiscus, Pavonia and Senra, four sutribe, two of them: Abutilinae (including depending on the anatomy of the plants, Abutilon) and Malvinae (including Altheae and Hibiscus separated from the other genera by Malva). the absence of trichomes on the stem and petiole, while in the three other genera; Fioria Fryxell (1988) reported the taxa of separated by the cross section of the stem Malvaceae in Mexico under four tribes where and petiole, presence of chlorenchyma and Hibiscus related to tribe Hibisceae, Pavonia number of the vascular bundles in petiole and related to tribe Malvavisceae, Abutilon presence of idioblasts. Despite the (Abutilon alliance) and Malva (Abutilon Malva) involvement of Hibiscus, Althaea and Malva related to tribe Malveae. species in the absence of leaf trichomes, but Fryxell (1997) depending on cpDNA, the former pieces differ from the others in the clarified that Althaea and Malva are related most studied anatomical attributes. genera, and also presented persuasive evidence for considering Fioria distinct from Acknowledgement: Hibiscus. This work was funded by Research and According to the anatomical results in Development Grants Program for National our studies, we agree with the Bayer and Research Institutes and Centers (GRANTS), Kubitzhi (2003) in the relationship between Graduate Research program, King Abdulaziz Althaea and Malva (due to the absence of City for Science and Technology (KACST), ducts and trichomes all over the plant, cross Kingdom of Saudi Arabia, grant number (1-18- section of the stem, shape of the epidermal 01-007-0001). cells, narrow cortex with the same components, wide pith, and the ground

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دراسات تشريحية مقارنة لبعض أنواع الفصيلة الخبازية من المملكة العربية السعودية وأهميتها التصنيفية إيمان قراقيش1، سعاد الرزيزا2، وقدري عبد الخالق2,3 1- قسم النبات، كلية العلوم، جامعة عين شمس، القاهرة، جمهورية مصر العربية 2- قسم االحياء، كلية العلوم التطبيقية، جامعة أم القري، مكة المكرمة، المملكة العربية السعودية 3- قسم النبات واالحياء الدقيقة، كلية العلوم، جامعة سوهاج، سوهاج، جمهورية مصر العربية تم في هذه الدراسة فحص الخصائص التشريحية لـ التشريحية في أعداد مفتاح تصنيفي لألنواع قيد الدراسة. 17 نوعا نباتيا ينتمي إلى سبعة أجناس من العائلة الخبازية اعتما د ا على وجود ،الشعيرات تنقسم األنواع المدروسة إلى الموجودة في المملكة العربية السعودية. ومن أهم مجموعتين رئيسيتين؛ تحتوي المجموعة األولى على the الصفات التي استخدمت في تحليل العالقة التطورية بين species of Althaea, Hibiscus and Malva )يعتمد تصنيفها األنواع المدروسة: شكل الساق والعنق واألوراق في على النظام الوعائي في الساق(، وتحتوي المجموعة المقطع العرضي، اشكال الشعيرات، البلورات، القنوات، الثانية على األجناس األربعة المتبقية حيث يعتمد تصنيفها األرومات األصيلة ذات الشكل النجمي، ونظام النسيج على العديد من السمات مثل المقطع العرضي للساق الوعائي الثانوي في الساق والعنق. استخدمت الصفات والعنق واألوراق وترتيب الشعيرات والقنوات.

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