Taxonomic studies in tribe Loteae (Fabaceae) in Egypt. I: Subtribe Anthyllidinae (Anthyllis, Hymenocarpos and Tripodion)

Abstract

The plant morphology, anatomical characters of stem and leaves, SEM of seed coat surfaces were used to reassess the conflicted taxonomic relationships between the genera Anthyllis, Hymenocarpos and Tripodion. Previous studies treated the genera Hymenocarpos and Tripodion as synonyms to Anthyllis. The present study clearly indicated considerably differences between the three genera. The most important characters used to distinguish the studied genera are habit, inflorescence type, bract shape, calyx, pod shape and seed coat pattern. On the bases of morphology, anatomy and seed characters, three distinct genera, Anthyllis, Hymenocarpos and Tripodion are represented in the Egyptian flora, each with only one species.

Full text

Egypt. J. Bot. Vol. 59, No.2, pp. 523 - 536 (2019)
#Corresponding author email: faizashehata@yahoo.com
DOI: 10.21608/ejbo.2019.5705.1234
Edited by: Prof. Dr. Fco Martin Huerta-Martinez, University of Guadalajara, Mexico
©2019 National Information and Documentation Center (NIDOC)
THE PLANT morphology, anatomical characters of stem and leaves, SEM of seed coat

Anthyllis, Hymenocarpos and Tripodion. Previous studies treated the genera Hymenocarpos
and Tripodion as synonyms to Anthyllis. The present study clearly indicated considerably
differences between the three genera. The most important characters used to distinguish the

On the bases of morphology, anatomy and seed characters, three distinct genera, Anthyllis,
Hymenocarpos and Tripodion 
Keywords: Anthyllis, Hymenocarpos, Tripodion, Morphological, Anatomy, SEM seed.
39
Introduction
The genus Anthyllis L. and Hymenocarpos Savi.
are two genera of the family Fabaceae, belonging
to the subfamily Faboideae Rudd., tribe Loteae
DC., subtribe Anthyllidinae W.D.J. Koch. The two
genera distributed in Mediterranean regions, with
some taxa extending into northern Europe, the
Atlantic islands, Northern and Eastern Africa, and
Western Asia (Polhill, 1981; Castroviejo, 2000 and
Sokoloff, 2003 a).
       
more or less exact vision of the genus Anthyllis
(syn. Vulneraria   
Linnaeus (1753) included 10 species under the
genus Anthyllis, of which A. tetraphylla and A.
vulneraria, and treated Hymenocarpos circinnatus
as Medicago circinnata. Medikus (1787) separated
Anthyllis tetraphylla as genus Tripodion, including
one species; T. tetraphylla.Savi (1798) separated
Medicago circinnata as genus Hymenocarpos,
including one species; H. circinnatus. He also
reported Anthyllis with two species; A. tetraphylla
and A. vulneraria.
Moench (1794) and Gussone (1827/28)
included Anthyllis tetraphylla as synonymy
to Vulneraria tetraphylla. Boissier (1838,
1839-1845) separated Anthyllis tetraphylla as
genus Physanthyllis, including one species; P.
tetraphylla. Boissier (1872) recognized Anthyllis
into A. vulneraria. H. circinnatus, H. nummularius
and P. tetraphylla. Taubert (1894) included
Hymenocarpos as synonymy to Circinus. Lassen
(1986, 1987) has shown that Tripodion is an earlier
name for Physanthyllis and recognized three
species in Tripodion. Akulova (1985, 1986) and
Sokoloff (2003 a, b) included Hymenocarpos as
synonymy to Anthyllis.
In Egypt, Täckholm (1974) recognized genus
Anthyllis into A. tetraphylla and A. vulneraria and
genus Hymenocarpos into H. circinnatus and H.
nummularius. El-Hadidi & Fayed (1994/95) and
Boulos (1995) recognized Tripodion tetraphyllum
as a separate genus and treated A. tetraphylla as a
synonym. Boulos (1999, 2009) treated Tripodion
tetraphyllum as a synonym to A. tetraphylla.
The present study aimed to revise critically the
taxonomic relationships between the species of
the related genera; Anthyllis, Hymenocarpos and
Tripodion in Egypt.
Materials and Methods
The present study is based on available fresh
material collected from their natural habitats
in Egypt in addition to collections kept in
    
of A. vulneraria and Tripodion tetraphyllum are
obtained from Institute of Plant Genetics and
Crop Research (IPK), Western Regional Plant
Introduction Station– Washington State University
and Desert Legume Program– The University of
Arizona (Table 1). The seeds were cultivated in
plastic house, till fruiting stage.
Taxonomic Studies in Tribe Loteae (Fabaceae) in Egypt. I: Subtribe
Anthyllidinae (Anthyllis, Hymenocarpos and Tripodion)
Zaki A. Turki, Faiza A. Shehata#, Esam M. Aqlan
Botany and Microbiology Department, Faculty of Science, Menoua University,
Shebein El-Koom, Egypt.

524 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
TABLE 1. Plant names, collection details and sources of seeds included in the present study.
Taxa Source of
seeds Localities Geographical
coordinates Date of collection
A. vulneraria PI 311348 - - -
Hymenocarpos
circinnatus -
Al-Mathani Al-Bahria - Marsa
Matrouh.
Wadi Umm El-Rakham – Marsa
Matrouh.
31° 27.963\ N
26° 45.287\ E
31° 24.076\ N
27° 01.704\ E
3,4 / 2014-2018
Tripodion tetraphyllum
Akz-Nr:
ANTHY 14
(IPK)
- - -
Samples for anatomy of the stem and mature
leaves were chosen from fresh materials. All
assessment was made on all plants at similar
developmental stages (fruiting stage) and in
comparable positions of each plant. Fresh
      
      

wax. The stems and leaves were sectioned at 10-

series. Sections were stained in safranin and light
green according to Sass (1961). The transverse
sections were examined and photographed by
Zeiss research microscope. A planimeter was used
for estimation of the width of each tissue in the
section. Terminology followed Abd El-Rahman
et al. (1976), Pandey (1982) and Abd El-Gawad
et al. (1989).
SEM study of the investigated seeds was
carried out by mounting mature seeds on brass
stubs and coated with a thin layer of gold using
JEOL JSM 530P SEM at the electron microscopic
unit, Faculty of Science, Alexandria University.
Terminology followed Lersten (1981), Brochmann
(1992), Stearn (1992) and Kirkbride et al. (2003).
Results
Macromorphological studies (Table 2 and Fig. 1)
Anthyllis vulneraria L., Sp. Pl. 719 (1753).
subsp. maura (Beck) Maire, Bull. Soc. Hist. Nat.
Afr. Nord 20: 20 (1929).
Syn. Anthyllis maura Beck, Ann. K. K.
Naturhist. Hofmus. 11: 64 (1896).
Perennial herb, 35-45cm height, stem
decumbent-erect, branched at base, tomentose,
cylindrical, whitish green, internodes up to 1mm
long in decumbent stem while 3-3.5cm long in
erect branches. Lower leaves simple, while upper
leaves imparipinnate, all leaves alternate, whitish
green, petiolate or sessile; petiolate leaves with
petioles 1.7-3.7cm long, puberulent; lamina in
simple leaf 4.2-4.5 × 0.8-0.9cm, narrow elliptic,
acuminate apex, entire margin, glabrous in
upper surface and tomentulose in lower surface;
imparipinnate leaves opposite-alternate with
     
       
    
unequal, narrow elliptic-elliptic acuminate-acute
apex, entire margin, glabrous in upper surface and
tomentose in lower surface; leaf rachis (4-) 14-


10-12cm long. Bracts palmatisect, 11-17mm
long, whitish green, pubescent in upper surface
but tomentose in lower surface; lower bracts 5-7
lobes while upper bracts 3 lobes, lobes elliptic-
lanceolate-oblong, 5-13 × 2-4mm, acute apex,
entire margin. Flowers 14.5-15mm long, pedicel
0.5-1mm long, tomentose; calyx tubular, with
oblique mouth, white with violet at apex, tube
7-9mm long, tomentose in outer surface, teeth
lanceolate-triangular, 1-2.5 mm long, unequal,
acute apex, entire margin, tomentose in outer
surface; standard purple white, lamina 13-14 ×
4.5-5mm, auriculate, entire margin, obtuse apex,
claw 6-6.5 mm long, veins violet, 2-3mm long,
glabrous; wings purple greenish white, lamina 12-
13 × 2-2.5mm, ovate, entire margin, rounded apex,
claw 8-8.5 mm long, auriculate 0.3-0.5 mm long,
truncate apex; keel greenish white, lamina 12-13 ×
1.5-2mm, straight apex, beak obtuse, dark violet,
claw 8-8.5 mm long. Androecium monadelphous,
       
      
above, anther uniform. Gynoecium stipitate,

525
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
9.5-12.5mm long, gynophore 1.5-2.5mm long,
glabrous; ovary 2 × 1mm, ellipsoid, glabrous,
style 7-8mm long, lower part thin and purple;
stigma capitates. Pod ellipsoid, 4-5 × 2.5-3mm,
pale brown-creamy, reticulate venation, included
within the calyx, beak 0.5-1mm long, seeds 1-2.
Seeds ovoid with rounded poles, 2-3 × 1-1.5mm,
brown or yellowish with terminal part pale green,
hilum subapical.
TABLE 2. Morphological characters of the studied taxa.
Character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum
Plant
Habit
Herb Herb Herb
Perennial Annual Annual
Decumbent-erect Decumbent Decumbent
Height (cm) 35-45 35-60 20-35
Colour Whitish green Whitish green Yellowish green
Stem
Shape Cylindrical Cylindrical Cylindrical
Surface Tomentose Pilose Pilose
Colour Whitish green Whitish green Reddish brown
Branched At base At base At base
Internode length (cm)
Up to 1 mm in decumbent
stem
3-3.5 in erect stem
3-6 1-2
Stipule Shape Filiform Absent Absent
Length (mm) Up to 0.5 - -
Leaf
Type
First - 2 Simple 2 Simple
Lower Simple Imparipinnate Imparipinnate
Upper Imparipinnate
Arrangement Alternate Alternate Alternate
Colour Whitish green Whitish green Yellowish green
Leaf rachis Length (mm) (4-) 14-25 5-15 3-5
Limb simple
leaf
Shape Narrow elliptic Obovate Elliptic
Size L × W (cm) 4.2-4.5 × 0.8-0.9 4-5.2 × 1.4-1.7 1.5-2 × 0.6-0.7
Apex Acuminate Acute-rounded Acute
Margin Entire Entire Entire
Surface Glabrous in upper
Tomentulose in lower Pilose in both Pilose in both

No. 3-9 2-7 2-5
Petiolule 0.5-1 mm Sessile Up to 0.5 mm
Opposite-alternate Opposite-alternate Alternate

Shape Narrow elliptic-elliptic Elliptic-obovate Elliptic-obovate
Size L × W (cm) Terminal 3-5.5 × 0.9-1.5
Lateral 0.5-3 × 0.3-0.7
Terminal 3-6 × 1-2.3
Lateral 0.7-2.6 ×
0.3-1.2
Terminal 1.2-2.5 × 0.7-1.2
Lateral 0.3-1.2 × 0.1-0.6
Apex Acuminate-acute Obtuse-acute Terminal rounded-truncate
Lateral acuminate-acute
Margin Entire Entire Entire
Surface Glabrous in upper
Tomentose in lower Pilose in both Pubescent in upper
Tomentulose in lower

526 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum
Petiole leaf Length (cm) 1.7-3.7 or sessile 1.5-2 Up to 0.5
Surface Puberulent Pilose Tomentulose
Peduncle Length (cm) 10-12 1-2 Sessile
Surface Tomentulose Pilose -
 Type Head Umbellate Cluster
 11-23 2-3 4-6
Bract
No. 1 1 1
Type Palmatisect Simple Simple
Shape 5-7 lobes and 3 lobes,
elliptic-lanceolate- oblong Elliptic Elliptic
Length (mm) 11-17 8.5-14 × 4-7 4.5-5.5 × 2-2.5
Lobe length (mm) 5-13 × 2-4 - -
Colour Whitish green Whitish green Green
Apex Acute Acute Acute
Margin Entire Entire Entire
Surface Pubescent in upper
Tomentose in lower Pilose in both Pubescent in both
Flower Length (mm) 14.5-15 6-7 14-18
Pedicel Length (mm) 0.5-1 0.5-1 0.5-1
Surface Tomentose Pilose Tomentose
Calyx
Colour White with violet apex Whitish green Greenish white with red
vein
Tube shape Tubular, with oblique
mouth Campanulate Tubular
Tube length (mm) 7-9 1-1.5 8-10
Tube surface Tomentose in outer Pilose in outer Tomentose in outer
Teeth shape Lanceolate -Triangular Linear Lanceolate
Teeth length (mm) 1-2.5 3-3.5 2.5-3
Teeth apex Acute Acute Acute
Teeth margin Entire Entire Entire
Teeth surface Tomentose in outer Pilose in outer Tomentose in outer and
inner
Standard
Shape Auriculate Circular pandurate
Colour Purple white Orangish yellow Greenish white
Lamina L × W (mm) 13-14 × 4.5-5 4-4.5 × 3.5-4 14.5-17 × 4.5-5.5
Claw length (mm) 6-6.5 0.5-1 8-10
Vein colour Violet Absent Crimson
Vein length (mm) 2-3 - 5-6
Margin Entire Entire Entire
Apex Obtuse Rounded Rounded
Surface Glabrous Glabrous Tomentose in outer
TABLE 2. Cont.

527
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
Character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum
Wings
Shape Ovate Oblong Ovate
Colour Purple greenish white Yellow Greenish yellow
Lamina L × W (mm) 12-13 × 2-2.5 4-4.5 × 1.5-2 12.5-15 × 2-2.5
Claw length (mm) 8-8.5 1-1.2 8-9
Apex Rounded Rounded Rounded
Margin Entire Entire Entire
Surface Glabrous Glabrous Glabrous
Auricule length (mm) 0.3-0.5 0.4-0.6 0.5-0.8
Auricule apex Truncate Rounded Truncate
Keel
Colour Greenish white Shiny yellow Greenish white
Lamina L × W (mm) 12-13 × 1.5-2 4.5-6 × 1.5-2 12-14 × 1.5-2
Claw length (mm) 8-8.5 1-1.5 9-9.5
Apex Straight beak, obtuse Straight beak, obtuse Straight beak, acute
Surface Glabrous Glabrous Glabrous
Beak colour Dark violet Yellow Dark violet
Androecium Type Monadelphous Diadelphous Diadelphous
Stamens
Free length (mm) - 3.5-4 10-13
Filaments united (free
parts length mm) 2-2.5 5 = 3-3.5
4 = 2-2.5 1-2
Filaments united (united
parts length mm) 9-10 2-2.5 9-11
Filament dilated above Filament dilated
above Filament dilated above
Anthers Uniform Uniform Uniform
Ovary
Shape Ellipsoid Narrow oblong Narrow oblong
Size L × W 2 × 1 1.2-1.5 × 0.5 3 × 0.5
Surface Glabrous Puberulent Puberulent in apex
Colour Green Green Light green
Gynophores Length (mm) 1.5-2.5 0.2-0.3 1.5-2
Surface Glabrous Glabrous Puberulent
Style Length (mm) 7-8 4-4.5 6-8
Lower part thin and purple Lower part thin Lower part thin
Stigma Shape Capitates Ellipsoid Capitates
Pod
Shape Ellipsoid Orbicular- reniform Ellipsoid - cylindrical
Size L × W (mm) 4-5 × 2.5-3 12-18 × 11-16 4-5.5 × 3-3.5
Colour Pale brown-creamy Blackish brown-pale
brown-brown Pale brown-creamy
Surface Reticulate Reticulate, appressed
hairy Reticulate, pubescent
Margin - Margins denticulate,
membranous wing -
Constriction - - Constricted between the
seeds
Included within the calyx - Included within the calyx
Beak length (mm) 0.5-1 - 2-3
Seed No. 1-2 2 1-2
TABLE 2. Cont.

528 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Fig. 1. Habit of the studied taxa: A. Anthyllis vulneraria; B. Hymenocarpos circinnatus; C. Tripodion tetraphyllum.
Hymenocarpos circinnatus (L.) Savi, Fl. Pis.
2:205 (1798).
Syns. Medicago circinnata L., Sp. Pl., ed.
1, 778 (1753). Medicago nummularia DC.,
Cat. Hort. Monsp. 124 (1813). Hymenocarpos
nummularis (DC.) G. Don, Gen. Hist. 2:173
(1832). Hymenocarpos nummularius (DC.) Boiss.,
Fl. Orient. 2:160 (1872). Cornicina circinnata (L.)
Boiss., Voy. Bot. Midi Esp. 2:163 (1839). Anthyllis
circinnata (L.) D.D. Sokoloff, Byull. Moskovsk.
Obshch. Isp. Prir., 108 (3):46 (2003).
Annual herb, 35-60cm height, stem decumbent,
branched at base, cylindrical, pilose, whitish green,
      
simple, alternate, whitish green, petiolate, petioles
1.5-2cm long, pilose, lamina 4-5.2 × 1.4-1.7cm,
obovate, acute-rounded apex, entire margin, pilose
in both surfaces; leaves imparipinnate, exstipulate,

petiolate- subsessile, elliptic-obovate, obtuse-
acute apex, entire margin, pilose in both surfaces,

       
  
 
Bracts simple, elliptic, 8.5-14 × 4-7mm, whitish
green, pilose in both surfaces, acute apex, entire
margin. Flowers 6-7mm long, pedicel 0.5-1mm
long, pilose; calyx whitish green, campanulate,
tube 1-1.5mm long, pilose in outer surface, teeth
linear, 3-3.5mm long, equal, acute apex, entire
margin, pilose in outer surface; standard orange-
yellow, lamina 4-4.5 × 3.5-4mm, circular, entire
margin, rounded apex, claw veinless, glabrous
0.5-1 mm long; wings yellow, lamina 4-4.5 × 1.5-
2mm, oblong, entire margin, rounded apex, claw
1-1.2mm long, auricule 0.4-0.6mm long, rounded
apex; keel shiny yellow, lamina 4.5-6 × 1.5-2mm,
straight apex, beak obtuse, claw 1-1.5mm long.
    
 
      

     
Gynoecium stipitate, 5.4-6.3mm long, gynophore
0.2-0.3mm long, glabrous; ovary 1.2-1.5 × 0.5mm,
narrow oblong, puberulent, style 4-4.5mm long,
lower part thin; stigma ellipsoid. Pod orbicular-
reniform, 12-18 × 11-16mm, blackish brown-
pale brown, reticulate venation, appressed hairy,
margins denticulate, membranous wing, with
two seeds. Seeds reniform, 3-3.5 × 2-2.5mm,
yellowish-creamy-pale brown, with rounded poles,
hilum blackish brown and lateral.
Tripodion tetraphyllum (L.) Fourr., Ann. Soc.
Linn. Lyon, ser. 2, 16:359 (1868).
Syns. Anthyllis tetraphylla L., Sp. Pl. 719
(1735). Vulneraria tetraphylla (L.) Guss., Fl. Sicul.
Prodr. 2:395 (1828-32). Physanthyllis tetraphylla
(L.) Boiss., Voy. Bot. Espagne 2:162 (1840).’
Annual herb, 20-35cm height, stem decumbent,
branched at base, cylindrical, pilose, reddish
      

529
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
leaves simple, alternate, yellowish green, petiolate,
petioles up to 0.5cm long, tomentulose; lamina 1.5-
2 × 0.6-0.7cm, elliptic, acute apex, entire margin,
pilose in both surfaces; leaves imparipinnate,
exstipulate, alternate, yellowish green, petiolate,
petioles up to 0.5 cm long, tomentulose; leaf 3-5
        


elliptic-obovate, rounded-truncate in terminal
     
entire margin, pubescent in upper surface while
tomentulose in lower surface; leaf rachis 3-5mm
     
Bracts simple, elliptic, 4.5-5.5 × 2-2.5mm, green,
pubescent in both surfaces, acute apex, entire
margin. Flowers 14-18mm long, pedicel 0.5-1
mm long, tomentose; calyx tubular, greenish white
with reddish at apex and veined, tube 8-10mm
long, tomentose in outer surface, teeth lanceolate,
2.5-3mm long, equal, acute apex, entire margin,
tomentose in both surfaces; standard greenish
white, lamina 14.5-17 × 4.5-5.5mm, pandurate,
entire margin, rounded apex, claw 8-10mm long,
veins crimoson, 5-6 mm long, tomentose in lower
surface; wings greenish white, lamina 12.5-15
× 2-2.5mm, ovate, entire margin, rounded apex,
claw 8-9mm long, auricule 0.5-0.8mm long,
truncate apex; keel greenish white, lamina 12-14
× 1.5-2mm, straight apex, beak acute, dark violet,
claw 9-9.5mm long. Androecium diadelphous,
       
        
   
uniform. Gynoecium stipitate, 10.5-13mm long,
gynophore 1.5-2 mm long, puberulent; ovary 3 ×
0.5mm, narrow oblong, puberulent in apex, style
6-8 mm long, lower part thin; stigma capitate.
Pod ellipsoid-cylindrical, 4.5-5 × 3-3.5mm, pale
brown-creamy, reticulate venation, pubescent,
constricted between the seeds, included within the
calyx, beak 2-3mm long, with 1-2 seeds. Seeds
oblong-ellipsoid crispate, 3-3.5 × 2-2.5mm, brown
with black spots, with rounded- truncate poles,
hilum lateral.
Anatomical studies
The anatomical investigations of the stem and
leaf of the studied taxa is represented in Tables 3,
4 and Fig. 2, 3.
Stem anatomy
Anthyllis vulneraria
Stem circular, 1.2-1.3mm diameter; epidermal

cuticle thickness. Cortex 7-8 parenchymatous

     





Hymenocarpos circinnatus
Stem circular, 1.9-2mm diameter; epidermal
    
     

 
     

 
      

diameter.
Tripodion tetraphyllum
Stem circular, 1.9-2.1mm diameter; epidermal
    
     
   
solitary crystals. Vascular cylinder 17-19 bundles,
     
     
  
     
      
   
solitary crystals. Tannin cells few in pith.
Leaf anatomy
Anthyllis vulneraria
The leaf in midrib region is v-shaped, 400-
     
    
     
    
     
      
     
       

main vascular bundles 3-4 layers of parenchyma
     

      
thickness, with solitary crystals.

530 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Stem character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum
Outline Circular Circular Circular
Diameter (µm) 1250-1275 1925-1970 1925-2025
Cuticle thickness (µm) 2.5-5 2.5-5 2.5-5
Epidermal
cell
Shape
Isodiametric-radially
elongated
Isodiametric-radially
elongated Isodiametric-radially elongated
Width (µm) 12.5-15 12.5-20 12.5-22.5
Cortex
Parenchyma number of
layers 7-8 5-6 7-9
Parenchyma Width
(µm) 100-137.5 112.5-175 200-370
Cell
shape
Isodiametric-tangentially
elongated Isodiametric Isodiametric-tangentially
elongated
Vascular bundles number 15-16 16-17 17-19
Vascular bundles width (µm) 150-200 220-300 140-270
 3-4 4-5 4-6
Pericyclic width (µm) 37.5-55 50-75 40-62.5
Phloem number of layers 3-4 4-5 3-4
Phloem width (µm) 20-30 35-50 25-37.5
Cambium number of layers 2 2 2
Cambium width (µm) 10-12.5 10-12.5 12.5-15
 2-7 2-5 2-8
 4-5 3-4 3-8
 100-160 100-150 60-150
Pith Cell shape Isodiametric-tangentially
elongated  
Diameter (µm) 520-530 1000-1025 950-975
Crystals In cortex Absent Absent Solitary
In pith Absent Absent Solitary
Tannin cells In cortex Absent Absent Absent
In pith Absent Absent Few
TABLE 3. Anatomical characters of stem in the studied taxa.
Hymenocarpos circinnatus
The leaf in midrib region is u-shaped, 450-
     
   

parenchyma 3-4 layers, angular-irregular, 120-
     
     


Below the main vascular bundles 3-4 layers of


chlorophyllous with wide air spaces, 5-6 rows,

Tripodion tetraphyllum
The leaf in midrib region is u-shaped, 480-
     

cuticle thickness. In midrib region, parenchyma

      
      
     
   
vascular bundles 4-5 layers of parenchyma cells,
     

consists of palisade and spongy tissues. Palisade
     


531
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
Character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum

Shape V U U
Midrib thickness (µm) 400-420 450-500 480-500
Cuticle thickness (µm) 2.5 2.5 2.5
Epidermal cells Thickness (µm) 12.5-25 up.
12.5-20 lo.
20-37.5 up.
12.5-22.5 lo.
25-40 up.
15-20 lo.
Shape Isodiametric-
tangentially elongated
Tubular-
tangentially
elongated
Isodiametric-tangentially
elongated
 4-6 3-4 5-6
 75-82.5 87.5-107.5 55-62.5
 2-6 3-5 2-3
Phloem number of layers 3-4 3-4 3-4
Phloem thickness (µm) 20-25 25-30 30-32.5
Parenchyma number of layers 2-3 up.
3-4 lo.
3-4 up.
3-4 lo.
3-4 up.
4-5 lo.
Parenchyma Thickness (µm) 87.5-100 up.
100-107.5 lo.
120-132.5 up.
112.5-125 lo.
112.5-125 up.
187.5-200 lo.
Cell shape  Angular-irregular Flattened-tangentially
elongated
Crystals Absent Absent Absent
 3-4 3-4 2-3
Fiber thickness (µm) 25-37.5 25-37.5 12.5-25
Tannin cells Upper vascular
bundle Absent Absent 2-3
Lower vascular
bundle
Absent Absent Absent

Thickness (µm) 300-350 280-310 220-230
Mesophyll with interspace
widely
Number of
rows 5-6 5-6 -
Thickness
(µm) 250-315 210-275 -
Palisade layer Number of
rows - - 2-3
Thickness
(µm) - - 62.5-85
Spongy layer Number of
rows - - 3-4
Thickness
(µm) - - 70-87.5
Tannin cells Absent Absent Absent
Crystals Solitary Absent Absent
TABLE 4. Anatomical characters of leaf in the studied taxa.
SEM of the spermoderm (Table 5 and Fig. 4)

and reticulation of their anticlinal (radial) walls,
the appearance of the outer periclinal walls and the
persistency of the primary cell walls.
Anthyllis vulneraria
Seed ovoid with rounded poles, 2-3 × 1-1.5mm
size, brown or yellowish with terminal part pale
green in colour, covered with wax, hilum circular,


Seed coat pattern irregularly reticulate, anticlinal
wall wavy, relief of cell boundary slightly channeled,
thickness of cell boundary moderate, curvature of
outer periclinal wall smooth and concave.

532 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Fig. 3. Leaf anatomy of the studied taxa, (A) Anthyllis vulneraria, (B) Hymenocarpos circinnatus, (C) Tripodion
tetraphyllum [ue= Upper epidermis, x= Xylem, p= Parenchyma; m= Mesophyll, pp= Palisade parenchyma, sp=
Spongy parenchyma, le= Lower epidermis, t= Tannin cell (x 50)].
Fig. 2. Stem anatomy of the studied taxa; (A) Anthyllis vulneraria, (B) Hymenocarpos circinnatus, (C) Tripodion
tetraphyllum 

533
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
TABLE 5. The morphological aspect of the spermoderm of the studied taxa.
Character Anthyllis vulneraria Hymenocarpos
circinnatus Tripodion tetraphyllum
Seed colour Yellowish with green in
terminal part - brown
Yellowish – creamy
– pale brown, hilum
blackish brown
Brown with black spots
Seed size L × W(mm) 2-3 × 1-1.5 3-3.5 × 2-2.5 3-3.5 × 2-2.5
L/W ratio 2 1.4 1.4
Seed pole Rounded Rounded Rounded- truncate
Seed shape Ovoid Reniform Oblong – Ellipsoid
Crispate
Seed coat pattern Reticulate Micropappilate in rows Papillae
Hilum
Position Subapical Lateral Lateral
Shape Circular Oblate Ovate
 83.87 × 80.65 75.81 × 88.71 83.87 × 77.42
Rim aril Raised Raised Raised
Micropyle Shape Obtriangular Narrow oblong Narrow oblong with one
open end
 7.8 × 7.8 7.8 × 1.56 9.36 × 1.56
Outline of cells Reticulate-irregular Oblong-radial elongated Tetra-hexagonal
Anticlinal wall Wavy Wavy Lobbed
Relief of cell boundary Slightly channeled Slightly channeled Channeled
Thickness of cell boundary Moderately Moderately Very thick
Curvature of outer periclinal wall Concave-smooth surface Concave-smooth surface Concave- irregular
Wax Present Present Present
Hymenocarpos circinnatus
Seed reniform, 3-3.5 × 2-2.5mm size, yellowish-
creamy-pale brown in colour with hilum blackish,
seed poles rounded. Seed coat pattern micropapilate
in rows, outline of cells oblong-radial elongated,
anticlinal wall wavy, relief of cell boundary slightly
channeled, thickness of cell boundary moderately,
curvature of outer periclinal wall concave, smooth

in position. Rim aril raised. Micropyle narrow

Tripodion tetraphyllum
Seed oblong-ellipsoid crispate, 3-3.5 × 2-2.5mm
size, brown with black spots in colour, seed poles
rounded-truncate. Seed coat pattern papillae in
rows, outline of cells tetra-hexagonal, anticlinal
wall lobbed, relief of cell boundary channeled,
thickness of cell boundary very thick, curvature
of outer periclinal wall concave irregular. Hilum
       
Rim aril raised. Micropyle narrow oblong with one

Discussion
Several attempts have been made in
     
Anthyllis, Hymenocarpos and Tripodion. Taubert
(1894) included Hymenocarpos as synonym
to Circinas. Sokoloff (2003 a) have treated
Hymenocarpos as synonym to Anthyllis (subgenus
Cornicina, section Hymenocarpos). Tikhomirov
& Sokoloff (1996), Benedi (2000) and Sokoloff
(2003 a) have treated Anthyllis tetraphylla as
genus Tripodion.
The morphological characteristics of the
studied taxa revealed that they varied from each
other and can be distinguished depending on the
    

The use of anatomical characters in taxonomic
investigation is becoming of increasing interest.
Anatomical structure is most likely providing
      
genera of uncertain taxonomic status, yet in the
same time proves very helpful for individual
     
Osmond et al., 1980). Turki (2007) and Kasem
(2016) reported the importance of anatomical
differences in the distinction among species.

534 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Fig. 4. SEM micrograph of spermoderm surface of the studied taxa; (A-D) Anthyllis vulneraria, (E-H)
Hymenocarpos circinnatus, (I-L) Tripodion tetraphyllum [A, E, I: Seed morphology; B, F, J: Hilum position; C, G,
K: Hilum shape; D, H, L: Spermoderm surface].
The studied taxa displayed remarkable
differences in the anatomical investigations
       
internal structure of the stems revealed differences
in cortex, number of vascular bundles, xylem, pith
diameter, crystals and tannin cells. Comparison
       
differences in shape and thickness of midrib and
xylem, lamina thickness, and crystals and tannin
cells.
Anticlinal undulations and characters of cell
boundaries in the seed exine are of high taxonomic
     
species and genus level (Barthlott & Voit, 1979
and Barthlott, 1981). Kaplan et al. (2007) and
Fawzi et al. (2010) reported seed coat characters
     

The results of spermoderm SEM revealed
differences in seed coat pattern, outline cells,
relief and thickness of cell boundary, curvature of
outer periclinal wall.
The present study, depending on the
results of macromorphological and anatomical
investigations, SEM studies on seeds clearly
indicates considerably differences between the
three studied genera Anthyllis, Hymenocarpos and
Tripodion and support the treatment of them as
different genera. The results agree with Medikus

535
Egypt. J. Bot. 59, No.2 (2019)
TAXONOMIC STUDIES IN TRIBE LOTEAE (FABACEAE) IN EGYPT...
(1787) in that Tripodion treated as a separate
genus.
Key to the genera
     
palmatisect, the leaf in midrib region is
v-shaped, hilum subapical in position, seed
coat pattern irregularly reticulate.. Anthyllis
- 
bract simple, the leaf in midrib region is
u-shaped, hilum lateral in position, seed coat
pattern otherwise …………………………...2
2- Flower 6-7mm long, calyx campanulate, pod
orbicular-reniform, cortex up to 6 layers, seed
coat pattern micropapilate……Hymenocarpos
- Flower 14-18mm long, calyx tubular, pod
ellipsoid- cylindrical, cortex 7-9 layers, seed
coat pattern papillae….…………... Tripodion
References
Abd El-Gawad, M.A., Salem, M.O. and Hegazi, A.M.
    
NPK-fertilization and saline irrigation. Ann. Agric.
Sci. Moshtohor, 27(3), 1439-1447.
Abd El-Rahman, A.A., Ibrahim, A.A. and Hassan, H.T.
(1976) Contribution to the anatomical characters
of some xerophytes. Bull. Fac. Sci. Cairo Uni. 49,
139-162.
Akulova, Z.V. (1985) To the question on ways of
morphological evolution in the genus Anthyllis
L. In: Anonymous (Ed.), Proceedings of 7th
Conference of Young Scientists of V.L. Komarov
Botanical Institute. VINITI, Moscow, pp. 29–36.
Akulova, Z.V. (1986) The Genus Anthyllis L. in the
Flora of USSR: Systematics, Morphology, and
Usage. Ph.D. Thesis, Leningrad (in Russian).
Barthlott, W. (1981) Epidermal and seed surface
characters of plants. Systematic applicability and
some evolutionary aspect. Nord. J. Bot. 1, 345-355.
Barthlott, W. and Voit, G. (1979) Mikromorphologie
der Samenschalen und Taxonomie der Cactaceae:
Ein rasterelectronen-mikroskopischer uberblick.
Plant Syst. Evol. 132, 205-229.
Benedi, C. (2000) Anthyllis, Hymenocarpos. In: "Flora
Iberica" Talavera, S. et al. (Eds.), pp. 829–862 and
868–873. 7(2). Real Jardin Botanico, Madrid.
Boissier, P.É. (1838) "Elenchus Plantarum Novarum...",
Genéve.
Boissier, P.É. (1839-1845) "Voyage Botanique dans le
Midi de l’Espagne". Vol. 2: 158-164. Paris.
Boissier, P.É. (1872) "Flora Orientalis". Vol. 2:156-
158.Basilea, Genéve, Lyon.
Boulos, L. (1995) "Flora of Egypt Checklist". Al-
Hadara Publishing, Cairo.
Boulos, L. (1999) "Flora of Egypt". Vol. 1.Al-Hadara
Publishing, Cairo.
Boulos, L. (2009) "Flora of Egypt Checklist", Revised
annotated edition. Al-Hadara Publishing, Cairo.
Brochmann, C. (1992) Pollen and seed anatomy of
Nordic Draba (Brassicaceae) phytogenetic and
ecological implications. Nordic J. Botany, 12(6),
657-673.
Castroviejo, S. (ed.) (2000) "Flora Iberica". Vol VII
(II) Leguminosae (Partim). Real Jardín Botánico
(CSIC), Madrid, Spain.
El-Hadidi, M.N. and Fayed, A.A. (1994/95) Material
for Excursion Flora of Egypt - Taeckholmia, 15,
1-223.
Fawzi, N.M., Fawzy A.M. and Mohamed, A.A.H.A.
(2010) Seed morphological studies on some species
of Silene L. (Caryophyllaceae). Inter. J. Bot. 6(3),
287-292.
Gussone, G. (1827/28) "Florae Siculae Prodromus".
Regia Typographia. Neapoli.
       
Morphological, anatomical and palynological
properties of some Turkish Veronica L. species
(Scrphulariaceae). Inter. J. Bot. 3(1), 23-32.
Kasem, W. (2016) Anatomical, pollen grains and seed
      Cleome L
(Cleomaceae Bercht. & Presl) collected from South
West of Saudi Arabia. J. Plant Sciences, 4, 29-36.
Kirkbride, J.H., Gunn, C.R. and Weitzman, A.L.
(2003) Fruits and seeds of genera in the subfamily

536 ZAKI A. TURKI et al.
Egypt. J. Bot. 59, No.2 (2019)
Faboideae (Fabaceae). United States Department
of Agriculture, Technical Bulletin 1208 No. 1890.
Lassen, P. (1986) In: "Hymenocarpos and Tripodion".
W. Greuter and T. Raus (Eds.), 16, pp. 111-112.
Med-Checklist notulae, 13. Willdenowia.
Lassen, P. (1987) In: W. Greuter & T. Raus (eds.), Med-
Checklist notulae, 14. Willdenowia 16: 443.
Lersten, N.R. (1981) Testa topography in Leguminoseae
subfamily Papilionoideae. Proc. Iowa Acad. Sci.
88(4), 180-191.
Linnaeus, C. (1753) Species plantarum, Vol II.
Stockholm, Sweden.
      
zu ordnen. Vorlesesungen der Churpf lzischen
physicalisch-conomischen Gesellschaft, 2, 354-
382.
Moench, C. (1794) A staminum situ describendi.
Methodus Plantas Horti Botanici et Agri
Marburgensis, 1, 1-368.
Osmond, C.B., Bjorkman and Anderson, D.J. (1980)
Physiological process in plant Ecology towards a
synthesis with Atriplex. – Berlin.
Pandey, B.P. (1982) "Plant Anatomy". New Delhi.
Polhill, R.M. (1981) Papilionoideae. In: " Advances
Legume Systematics", R.M. Polhill and P.H. Raven
(Eds.), part 1, pp. 191-208. Royal Botanic Gardens,
Kew.
Sass, J.E. (1961) "Botanical Microtechnique", 3rd ed. –
Amsterdam.
Savi, G. (1798) "Flora Pisana", Vol. 1-2. Pietro
Giacomelli Editore, Pisa.
Sokoloff, D.D. (2003 a) On system and phylogeny of
the tribe Loteae DC. (Leguminosae) [in Russian].
Bulletin of Moscow Society of Naturalists,
Biological Series, 108(3), 35-48.

of the Tribe Loteae DC. of the Family Leguminosae.
Ph.D. Thesis, Moscow (in Russian).
Stearn, W.T. (1992) "Botanical Latin", 4th ed. Timber
Press, Oregon, USA.
Täckholm, V. (1974) "Students’ Flora of Egypt". 2nd ed.,
Cairo University, Egypt.
Taubert, P. (1894) In: "Leguminosae". Engler, A.,
     
Engelmann, Leipzig, pp. 70-385.
Tikhomirov, V.N. and Sokoloff, D.D. (1996) On the
division of the genus Anthyllis L. (Papilionaceae,
Loteae) into subgenera and sections. Bulletin of
Moscow Society of Natura;ists, Biological Series,
101, part 1, 61-73 (in Russian).
Tournefort, J. (1719) Institutione rei herbariae, 3rd ed.,
Paris.
Turki, Z.A. (2007) The genus Ammannia L. (Lythraceae)
in Egypt. Flora Mediterranea, 17, 97-114.
Welkie, J.T. and Caldweli, M. (1970) Leaf anatomy of
species in some dicotyledon. Families as related to
Canad.
J. Bot. 48, 2135-2146.
(Received 24/10/2018;
accepted 27/3 /2019)
Loteae
(Anthyllis, Hymenocarpos  Tripodion) Anthyllidinae


   Hymenocarpos Anthyllis         
 Tripodion
.
Hymenocarpos
HymenocarposAnthyllisAnthyllis Tripodion
 Tripodion