Phylogenetic Relationships in Artemisia spp. (Asteraceae) Based on Distribution of Foliar Trichomes

Abstract

The phylogenetic relationships within the genus Artemisia have been very controversial and need throughout investigations. In continuation to the previous paper, here we report the phylogenetic relationships in the genus Artemisia based on the foliar trichomes using light microscopy and scanning electron microscopy. The data from 24 taxa was analyzed for its phylogeny. In addition, eight new types of foliar trichomes in the genus were described. This study also revealed that foliar trichomes of the genus Artemisia are good taxonomic markers and can be utilized to resolve the taxonomic conflicts within the genus.

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INTERNATIONAL JOURNAL OF AGRICULTURE & BIOLOGY
ISSN Print: 1560–8530; ISSN Online: 1814–9596
09–174/MHB/2009/11–5–553–558
http://www.fspublishers.org
Full Length Article
To cite this paper: Hayat, M.Q., M. Ashraf M.A. Khan, G. Yasmin, N. Shaheen and S. Jabeen, 2009. Phylogenetic relationships in Artemisia spp.
(Asteraceae) based on distribution of foliar trichomes. Int. J. Agric. Biol., 11: 553–558
Phylogenetic Relationships in Artemisia spp. (Asteraceae) Based
on Distribution of Foliar Trichomes
MUHAMMAD QASIM HAYAT1, MUHAMMAD ASHRAF†, MIR AJAB KHAN, GHAZALAH YASMIN, NIGHAT SHAHEEN,
AND SHAZIA JABEEN‡
Department of Plant Sciences, Quaid-i-Azam University, Islamabad, Pakistan
†NUST Center of Virology and Immunology, National University of Science and Technology, Rawalpindi, Pakistan
‡National Center of Excellence in Geology, University of Peshawar, Peshawar, Pakistan
1Corresponding author’s e-mail: mqasimhayat@hotmail.com
ABSTRACT
The phylogenetic relationships within the genus Artemisia have been very controversial and need throughout investigations. In
continuation to the previous paper, here we report the phylogenetic relationships in the genus Artemisia based on the foliar
trichomes using light microscopy and scanning electron microscopy. The data from 24 taxa was analyzed for its phylogeny. In
addition, eight new types of foliar trichomes in the genus were described. This study also revealed that foliar trichomes of the
genus Artemisia are good taxonomic markers and can be utilized to resolve the taxonomic conflicts within the genus.
Key Words: Artemisia; Seriphidium; Anthemideae; Asteraceae; Anatomy; Trichomes; Phylogeny
INTRODUCTION
Artemisia L. is one of the largest genera of the family
Asteraceae. Its members are wind pollinated and mainly
distributed in temperate areas of mid to high latitudes of the
northern hemisphere, colonize in arid and semiarid
environments, and only few representatives are found in
southern hemisphere (McArthur & Plummer, 1978; Valles
& McArthur, 2001). Many species of the genus have
economic value as medicines, food, forage, ornamentals or
soil stabilizers in disturb habitats; some taxa are toxic or
allergenic and some others are invasive weeds, which can
adversely affect harvests (Pareto, 1985; Tan et al., 1998;
Hayat et al., 2009a & b). Except few annuals or biannual,
most Artemisia species are perennial (Valles et al., 2003).
The genus Artemisia is also considered as indicator of
steppe climate (Erdtman, 1952) and moderate precipitation
(El-Moslimany, 1990).
Classically the genus has been divided into four
groups, which has been treated as sections or subgenera;
Absinthium (Tournefort) de Cand., Artemisia Tournefort
(=Abrotanum Besser), Dracunculus Besser, Seriphidium
Besser (Hooker, 1881; Martin et al., 2001 & 2003).
McArthur et al. (1981) proposed a new group Tridantatae
(Rydb.) McArthur, which is endemic to North America.
Ling (1982, 1991a & b, 1995a & b) separated Seriphidium
(Besser ex Hooker) as independent genus. Bremer and
Humphries (1993) and Bremer (1994) accepted this
separation. But Kornkven et al. (1998), Torrell et al. (1999)
and Watson et al. (2002) in their molecular studies again
merged Seriphidium with Artemisia. Nonetheless
classification of Artemisia and relationships among its
different taxa are still controversial.
Scotland et al. (2003) opined that rigorous and critical
anatomical studied of fewer morphological characters in the
context of molecular phylogenies is fruitful to integrating
the strengths of morphological data with those of sequence
data. Since the micromorphological characteristics of foliar
trichomes play an important role in plant taxonomy,
especially of particular groups at generic and specific levels,
attention of plant morphologists and systematists has been
mainly attracted to resolve the taxonomic conflicts (Hardin,
1979; Fang & Fan, 1993). Although many studies
conducted on the histochemistry of the secretory products of
the glandular trichomes of Artemisia (Smith & Kreitner,
1983; Slone & Kelsey, 1985; Ascensao & Pais, 1987; Duke
& Paul, 1993; Duke et al., 1994), little is known about the
systematic significance of trichomes in Artemisia. In the
present paper, we report the micromorphological
characteristics of foliar trichomes in Artemisia using light
microscopy (LM) and scanning electron microscopy (SEM).
The specific objectives were to: (a) identify and compare the
micromorphological characteristics of foliar trichomes in
different species of this genus and (b) reconstruct the
phylogenetic relationships among different taxa of
Artemisia based on characteristics of foliar trichomes.
MATERIALS AND METHODS
All details about the origin and collection of leaf
material, processing of the tissues, basic terminology and
studies of the foliar trichomes were essentially the same as

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554
we reported in the previous paper (Hayat et al., 2009a).
Source and collection information of remaining taxa is
given in Table I. Using modified methodology of Shaheen
et al. (2009) and Yasmin et al. (2009) foliar trichomes were
at first examined by OLYMPUS/BX-51 light microscope.
Pieces of leaves were dipped in 30% Nitric acid and boiled
along with 1.5 g of Potassium chloride in a test tube for 2-3
min. Then these leaf pieces were cleaned with distal water.
Epidermis was removed and kept in 60% Potassium
hydroxide solution for 2 h. Finally, these leaf sections were
suspended in Lactic acid and transferred on glass slides for
LM observations. For SEM investigations, the dried leaves
were mounted on aluminum stubs with the help double
adhesive tape, sputter coated with gold by SPI-Module
Sputter Coate and studied with a Jeol-JSM 5910 scanning
electron microscope. Basic terminology used for trichomes
categorization and elaboration was that recommended by
Ramayya (1972), Payne (1978), Bento et al. (2008), Popa
and Sipos (2009) and Shaheen et al. (2009). However,
straightforward self illustrative terms are incorporated to
recognize the particular type of trichome.
On the bases of presence or absence, all 16 foliar
trichomes types, noted here, were selected as a character
states for phylogenetic analysis of Artemisia (Table II). The
plesiomorphic or apomorphic state of each trichome was
determined using the criteria established by Boudreaux
(1979) and further explained by Crisci and Stuessy (1980).
In this study an imaginary outgroup was used for
comparison that contained all the ancestral characters. An
original binary data matrix was produced (Table III) for
phylogenetic analysis using the outgroup comparison
method (Watrous & Wheeler, 1981). The phylogenetic
analysis was done by PHYLIP computer program version
3.67 (Felsenstein, 2007). Most parsimonious trees (MPTs)
based on the binary matrix were constructed with MIX
program of PHYLIP using Wagner parsimony method
(Farris, 1970). A strict consensus phylogenetic tree of the
MPTs was generated using the CONSENSE program of
PHYLIP (Sokal & Rohlf, 1981). Finally, using
DRAWTREE and DRAWGRAM programs of PHYLIP
strict consensus phylogenetic tree of Artemisia were
generated.
RESULTS
Types of foliar trichomes. Based on observations of LM
(Fig. 1) and SEM (Fig. 2), the foliar trichomes in 24 taxa
from Artemisia were classified into 16 main types. Of these
a-h were described in Hayat et al. (2009a), i-p are
illustrated below:
(i). Vase-shape trichomes. These are glandular
trichomes. They are cylindrical in shape with constricted
apex and are characteristic of A. persica (Fig. 1A & Fig.
2A).
(j). Aduncate curly trichomes. These are also non-
glandular trichomes. They are long cylindrical in shape.
They are characteristic feature of A. roxburghiana (Fig. 1B).
(k). Dolabrate trichomes. They have shape like the head
of pick, with two divaricated or opposed terminal branches.
These non-glandular trichomes are found in A. vulgaris
(Fig. 1C).
(l). Unicellular peltate trichomes. These glandular
trichome are embedded in epidermis and are the
characteristic feature of A. vulgaris (Fig. 1D), A.
roxburghiana and A. japonica.
(m). Rope rolled trichomes. These are nonglandular
trichomes. They are exclusive characteristic feature of A.
moorcroftiana (Fig. 2B).
Fig. 1. Types of glandular and nonglandular foliar
trichomes in Artemisia by means of LM: A, A. persica;
B, A. roxburghiana; C-D, A. vulgaris (Scale bar = 50
µm)
Fig. 2. Types of glandular and nonglandular foliar
trichomes in Artemisia by means of SEM: A, A. persica
(Scale bar = 10 µm); B, A. moorcroftiana (Scale bar =
10 µm); C, S. kurramense (Scale bar = 10 µm); D, A.
stricta (Scale bar = 1 µm)

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(n). Cylindrical trichomes. They are cylindrical in shape.
These non-glandular trichomes are the unique feature of S.
kurramense (2C).
(o). Floriform peltate trichomes. These glandular
trichomes have flower like appearance and are present in A.
stricta (Fig. 2D).
(p). Cup-shape peltate trichomes. They are unicellular
cup like glandular structures with broad apical opening.
They are found in A. tangutica (Fig 3).
The quantitative dimensions of all the trichomes types
studied are given in Table IV and V.
Phylogenetic analysis. Hundred MPTs were generated
using Wagner parsimony method (Farris, 1970) and then a
strict consensus phylogenetic tree of these MPTs was
obtained (Fig. 4 & Fig. 5). In the resulting phylogenetic tree,
Artemisia and Seriphidium is shown to be a monophyletic
group.
DISCUSSION
Features of trichomes are generally considered as
valuable for ascertaining the taxonomic relations within the
genus Artemisia (Hall & Clements, 1923). Different forms
are reported to occur in different taxa of Artemisia (Ferreira
& Janick, 1995). Different authors reported only two types
of trichomes in the genus Artemisia: a) capitate glandular
trichomes (Smith & Kreitner, 1983 in A. ludoviciana Nutt.;
Kelsey, 1984 in A. nova Nelson; Slone & Kelsey, 1985 in A.
tridentata Nutt.; Ascensao & Pais, 1987 in A. compestris L.;
Lodari et al., 1989 in A. princeps Pamp.; Ferreira & Janick,
1995 in A. annua) and b) T-shape nonglandular trichomes
(Ascensao & Pais, 1987 in A. compestris ; Lodari et al.,
1989 in A. princeps, A. absinthium, A. capillaris & A.
japonica; Ferreira & Janick, 1995 in A. annua). In this and
our previous paper (Hayat et al., 2009a), we reported not
only 16 new types of glandular and non-glandular foliar
trichomes in Artemisia but also un-veiled the under lying
variations in capitate and T-shape trichomes of the genus.
In addition to capitate and T-shape trichomes and
those described in Hayat et al. (2009a), here we also
observed eight new types of trichomes of taxonomic
importance. Of these, unicellular peltate trichomes of A.
vulgaris (Fig. 1D), A. roxburghiana and A. japonica, vase-
shape trichomes (Fig. 1A & 2A) of A. persica; aduncate
curly trichomes (Fig. 1B) of A. roxburghiana; dolabrate
trichomes (1C) of A. vulgaris; rope rolled trichomes (Fig.
Table I*. List of taxa studied for foliar anatomy and their herbarium vouchers. ISL: Herbarium, Quaid-i-Azam
University, Islamabad. PUP, Herbarium, University of Peshawar, Peshawar
Taxon Collection data Herbarium Voucher
Section Artemisia Tournefort
A. rutifolia Spreng. Gilgit: Nattar valley. A. Rashid, 1988. PUP, 244 (1105)
A. santolinifolia Turcz. ex Krasch. Gilgit: Nattar valley. A. Rashid, 1986. PUP, 239 (1108)
A. vestita Wall. ex DC. Jahlum: Soon vally, Sakasar. M. Farooq, 2005. ISL, 20093
Section Seriphidium (Besser) Besser
A. maritima L. Skardu: M. Q. Hayat, 2007. PUP, PH003 (ART003)
S. brevifolium (Wall. ex DC.) Ling & YR Ling Mansehra: Ujtar, Naran to Lalusar lake track. M. Q. Hayat, 2007. PUP, PH007 (ART007)
S. stenocephalum (Krasch. ex Poljakov) Poljakov Gilgit: Chalas. M. Q. Hayat, 2008. PUP, PH010 (ART010)
S. turanicum (Krasch.) Poljakov Gilgit: Nattar vally. M. Q. Hayat, 2008. PUP, PH009 (ART009)
Section Dracunculus Besser
A. scoparia Waldst. et Kit. Islamabad: Quaid-i-Azam university campus. M. Q. Hayat, 2008. ISL, 32313
A. stricta Edgew. Kashmir: Muzafrabad. T. Malik, 1972. ISL, 25650
*Partly adapted from Table I, Hayat et al. (2009a)
Table II. Character and character states of foliar
trichomes for the phylogenetic analysis of Artemisia
(the number in brackets represents the codes of
character states; plesiomorphic, 0; apomorphic, 1)
Charecter Character states
a. Capitate Present (0), Absent (1)
b. Pluricellular Absent (0), Present (1)
c. Multicellular peltate Absent (0), Present (1)
d. Thin neck Absent (0), Present (1)
e. T-shape Present (0), Absent (1)
f. Macroform Absent (0), Present (1)
g. Unicellular tector Absent (0), Present (1)
h. Clavate Absent (0), Present (1)
i. Vase-shape Absent (0), Present (1)
j. Aduncate curly Absent (0), Present (1)
k. Dolabrate Absent (0), Present (1)
l. Unicellular peltate Absent (0), Present (1)
m. Rope rolled Absent (0), Present (1)
n. Cylindrical Absent (0), Present (1)
o Floriform peltate Absent (0), Present (1)
p. Cup-shape peltate Absent (0), Present (1)
Fig. 3. Types of glandular foliar trichomes in Artemisia
by means of LM: A. tangutica (Scale bar = 50µm)

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2B) of A. moorcroftiana; cylindrical trichomes (Fig. 2C) of
S. kurramense; floriform trichomes (Fig. 2D) of A. stricta
and cup-shape peltate trichomes (Fig. 3) of A. tangutica, are
important one.
He et al. (2000) resolved the taxonomic conflicts in
the genus Actinidia Lindl. and related taxa by following the
same methodology. In this paper, the results obtained from
the phylogenetic tree (Fig. 4 & Fig. 5) based on the
micromorphological characteristics of foliar trichomes
support the view presented based on molecular studies
(Kornkven et al., 1998; Torrell et al., 1999; Watson et al.,
2002) that Artemisia and Seriphidium are monophyletic
groups.
From cladogram (Fig. 4) and phylogenetic tree (Fig. 5)
it is clear that foliar trichome evolution in Artemisia starts
form outgroup (assumed as ancestor of Artemisia). The first
evolved group (1) consist of those taxa, which have both T-
shape and capitate trichomes. The second evolve group (2)
has only capitate trichome and third group (3) is without
trichomes. A possible tendency for foliar trichome evolution
is marked in Fig. 4 and Fig. 5. Also we support the idea
about general degenerate evolutionary tedency of
Asteraceae (Gailing & Bachmann, 2003). we do not believe
on old classification of the genus, because it was based only
on floral characters and has many objections; for example
section Artemisia only differ from section Absinthium by a
Table III. Data matrix used in phylogenetic analysis of Artemisia (Character & character states are described in
Table II)
Taxon Abbreviation Trichomes*
a b c d e f g h i j k l m n o p
Outgroup Out 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. amygdalina Amy 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. biennis Bie 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. dubia Dub 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0
A. moorcroftiana Moo 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0
A. roxburghiana Rox 1 1 0 0 0 0 0 1 0 1 0 1 0 0 0 0
A. rutifolia Rut 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. santolinifolia San 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. tournefortiana Tou 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0
A. vestita Ves 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. vulgaris Vul 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0
A. absinthium Abs 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. macrocephala Mac 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. persica Per 0 0 1 1 1 1 0 0 1 0 0 0 0 0 0 0
A. siversiana Siv 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. tangutica Tan 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1
A. maritima Mar 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
S. leucotrichum Leu 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
S. brevifolium Bre 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
S. kurramense Kur 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0
S. stenocephalum Ste 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0
S. turanicum Tur 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
A. japonica Jap 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
A. scoparia Sco 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0
A. stricta Str 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0
*a, capitate; b, Pluricellular; c, multicellular peltate; d, thin neck; e, T-shape; f, macroform; g, unicellular tector; h, clavate; i, vase-shape; j, aduncate curly;
k, dolabrate; l, unicellular peltate; m, rope rolled; n, cylindrical; o, floriform peltate; p, cup-shape paltate
Table IV. Quantitative characteristics of glandular foliar trichomes of Artemisia
Taxa Vase-shape Unicellular peltate Floriform peltate Cup-shape peltate
Height x width (µm) Diameter (µm) Diameter (µm) Diameter (µm)
A. roxburghiana Absent 10-14 Absent Absent
A. vulgaris Absent 10-15 Absent Absent
A. persica 97-101x45-50 Absent Absent Absent
A. tangutica Absent Absent Absent 20-25
A. japonica Absent 9-13 Absent Absent
A. stricta Absent Absent 4-5 Absent
Table V. Quantitative characteristics of nonglandular foliar trichomes of Artemisia
Taxa Aduncate Dolabrate Rope rolled Cylindrical
Height × width (µm) Height × width (µm) Height × width (µm) Height × width (µm)
A. moorcroftiana Absent Absent 200-250x45-50 Absent
A. roxburghiana 700-750x15-20 Absent Absent Absent
A. vulgaris Absent 25-30x10-15 Absent Absent
S. kurramense Absent Absent Absent 35-40x8-10

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single character i.e., receptacle naked (Artemisia) or
receptacle cover with long hairs (Absinthium) (Kaul &
Bakshi, 1984). However, we believe that more taxa of the
genus Artemisia, which includes sufficient taxa of each
classical section, need to be investigated in more detail and
especially focusing on the micromorphological characters of
foliar trichomes integrated with molecular approaches.
In conclusion, diversity in glandular and non-glandular
foliar trichomes is a valuable taxonomic tool. Non-etheless,
there is a need to develop better terminology and detail
comparative study of these micromorphological features to
resolve taxonomic conflicts in the genus. Their careful
anatomical and ontological studies along with the
integration of molecular data one can portray the complete
picture about the infrageneric classification of Artemisia.
Acknowledgement. We are grateful to Dr. Riaz and Mr.
Abdullah Jan, Department of Physics and Dr. M. Tahir
Shah, NCE in Geology, University of Peshawar, Pakistan
for their facilitation. We also acknowledge HEC Pakistan
for their financial assistance.
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(Received20 May 2009; Accepted 29 May 2009)