Advances in Bioscience and Biotechnology, 2013, 4, 15-20 ABB
http://dx.doi.org/10.4236/abb.2013.410A3003 Published Online October 2013 (http://www.scirp.org/journal/abb/)
Homeobox leucine zipper proteins and
Muzna Zahur1,2*, Muhammad Ahsan Asif1, Nadia Zeeshan1, Sajid Mehmood1,
Muhammad Faheem Malik1, Abdul R. Asif3
1Department of Biochemistry and Molecular Biology, University of Gujrat, Gujrat, Pakistan
2Department of Neurology, University Medical Center Goettingen, Goettingen, Germany
3Department of Clinical Chemistry, University Medical Center Goettingen, Goettingen, Germany
Received 7 July 2013; revised 7 August 2013; accepted 1 September 2013
Copyright © 2013 Muzna Zahur et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Transcription factors play key roles in plant develop-
ment and stress responses through their interaction
with cis-elements and/or other transcription factors.
Homeodomain associated leucine zipper proteins
(HD-Zip) constitute a family of transcription factors
that are characterized by the presence of a DNA-
binding domain closely linked with leucine zipper
motif functioning in dimer formation. This type of
association is unique to plants and considered as an
excellent candidate to activate developmental respons-
es to altering environmental conditions. Cotton is the
most important fiber plant with a lot of local and
commercial uses in the world. HD-Zip proteins not
only have key roles in different stag es of vascular and
inter-fascicular fiber differentiation of cotton but also
are suggested to have an important role against abio-
tic stress that is one of the key factors limiting cotton
productivity. Plants have developed various strategies
to manag e stress cond itions through a combination of
metabolic, physiological and morphological adapta-
tions. These adaptive changes rely largely on altera-
tions in gene expression. Therefore, transcriptional
regulators play a crucial role in stress tolerance. Be-
ing a transcription factor HD-Zip might be a useful
target for genetic engineering to generate multiple
stress tolerance in susceptible plants. In the following
chapter, we discussed how the HD-Zip proteins would
play a useful role for cotton development both in fiber
production and stres s adaptati on .
Keywords: Cotton; Stress; Transcription Factor;
HD-Zip Proteins; Homeobox Leucine Zipper
1. ENVIRONMENTAL STRAINS AND
Plants are exposed to a variety of stress factors that pre-
vent them from attaining their full genetic potential. This
can be due to insects, fungal infections, weeds, bacteria
or viruses, all of which are known as biotic factors. The
abiotic stress factors include drought, salinity, flooding,
oxidative stress, heavy metal, cold and high temperature
[1,2]. Abiotic stress, in fact, is the major cause of crop
failure worldwide. It dips average yields for most major
crops by more than 50% .
When plants are subjected to the stress, they respond
through various cellular signal transduction pathways,
which result in accumulation of certain differentially ex-
pressed gene products that can be classified as functional
and regulatory proteins. Functional proteins include wa-
ter channel proteins, key enzymes for osmolyte biosyn-
thesis, chaperones, LEA (late embryogenesis abundant)
proteins, proteinases and detoxicating enzymes. Regula-
tory proteins include transcription factors, protein kinas-
es, and phospholipases. Regulatory proteins are involved
in the further regulation of signal transduction and gene
expression of stress tolerant proteins [4-7]. Improving
the crop plant potential to endure different abiotic stress-
es will lead to more yields by either enhancing the crop
set or expanding crop cultivation in the areas previously
refuted due to stress intolerance.
2. GOSSYPIUM (COTTON)
Cotton is an important cash crop known as white gold
due to its valuable fiber production and oilseeds . A
large number of ginning factories and textile mills great-
ly depend upon cotton. However, Cotton yield is greatly
affected by many factors, such as the variety grown, cul-
tivation method, environmental and climatic conditions,
M. Zahur et al. / Advances in Bioscience and Biotechnology 4 (2013) 15-20
amount and application strategy of fertilizers, time of
sowing and availability of irrigation water .
There are 50 diverse species of the genus Gossypium.
Four species are cultivated, G. hirsutumL. and G. barba-
dense L., that are tetraploid (2n = 4x = 52), and G. arbo-
reum L. and G. herbaceum L., that are diploid (2n = 2x =
26). The most extensively cultivated species throughout
the world is G. hirsutum. Whereas the diploid cotton spe-
cies are a pool for important disease resistance and pest
control genes, and improved agronomic and fiber quail-
ties but also have better opportunities for structural and
functional studies of genes through advanced systems of
gene knockouts . Asiatic G. arboretum L (Desi cot-
ton.) has built-in desirable genes for drought tolerance
and resistance to insect pests like bollworms, aphids and
diseases like black arm, root rot, reddening of leaves and
most importantly, highly destructive leaf curl disease of
cotton. Its diploid genome makes it a good choice for the
identification of novel genes in genus Gossypium .
Some of the cotton genotypes are more tolerant through
an intricate set of genetic parameters including sensing,
signal transduction and response. Due to the large num-
ber of genes participating in response to an external
stress, improvement through conventional breeding is
very difficult. Conventional breeding has developed many
new cultivars and varieties; however it has some limita-
tions like thousands of genes getting transferred in each
cross and the barriers for gene transfer through incom-
patibility and species differences . Genetic engineer-
ing technology has made possible the insertion of desired
foreign gene(s) to overcome problems of sexual incom-
patibility and species barriers between organisms. This
technology helps the breeders and molecular biologists to
introduce only the gene of interest with more selective
modification and represents a significant advance . In
this background we require those cotton varieties which
resist these biotic and abiotic stresses. This resistance in
cotton to various stresses can be gained by improving the
cotton plant through stress resistant genes with special
emphasis on stress responsive transcription factors con-
trolling the multiple genes involved in stresses . Se-
veral stress responsive transcription factor genes have
been identified in G. hirsutum and G. arboreum such as
WRKY, EREBP, NAC, HD-Zip and DREB genes [15-
3. TRANSCRIPTION FACTOR (TF)
Transcription factors are the sequence-specific DNA bin-
ding proteins that control the transfer of genetic informa-
tion from DNA to mRNA . These are the first line of
defense against stress stimuli that in turn activate the
expression of other stress responsive genes. These tran-
scription factors bind to the specific elements in the pro-
moter regions called cis-acting elements and the tran-
scription factors that bind to these elements are known as
trans-acting factors. Several cis-acting promoter ele-
ments and their subsequent binding proteins, each con-
taining a distinct type of DNA binding domain, such as
AP2/ERF, basic leucine zipper, HD-ZIP, MYB, MYC,
and several classes of zinc finger domains, have been in-
volved in plant stress responses due to their variable ex-
pression under different stress conditions . Combina-
torial interactions of promoters DNA cis-acting elements
with trans -acting protein factors are chief processes gov-
erning spatio-temporal gene expression .
Most of the transcription factors are common among
different plants in their motif structure and mode of ac-
tion . These are potent targets for genetic engineering
of stress tolerance because a transcription factor is en-
coded by a single gene but regulates the expression of se-
veral other genes leading to the activation of complex
adaptive mechanisms. Therefore, in transgenic plants
transcription factors can confer better stress tolerance
than a single gene transfer. This opens an excellent op-
portunity to develop stress tolerant crops in future that
can contribute to sustainable food and fiber production in
the world .
Several transcription factor proteins have been identi-
fied from different Gossypiun species and analyzed for
their role in diverse stress and development conditions. A
leucine zipper-containing WRKY protein named
GaWRKY1 was isolated from G. arboreum using the
CAD1-A, (a gene contributing in cotton sesquiterpene
biosynthesis) promoter. In transgenic Arabidopsis plants
and transiently transformed tobacco leaves expression of
GaWRKY1 triggered expression of the CAD1-A pro-
moter, and interruption of the W-box abolished the acti-
vation . Duan et al.  isolated two EREBP (ethyl-
ene response element binding protein) genes named
GhEREB2 and GhEREB3 suggesting their role as the
positive transcription factors in biotic stress (ethylene
and jasmonic acid) signal transduction pathways. A
DRE-binding protein, GhDBP2, was isolated from G.
hirsutum seedlings that participate in the activation of
down-stream genes in response to environmental stresses
and ABA treatment . Another DRE binding protein,
GhDREB, containing a conserved AP2/EREBP domain
reported in G. hirsutum that is induced by drought, high
salt and cold stresses in seedlings. GhDREB accumulates
higher levels of soluble sugar and chlorophyll in leaves
following to drought, high salt, and freezing stress treat-
ments in transgenic wheat plants conferring enhanced to-
lerance . From the NAC (NAM, ATAF1, −2, and
CUC2) gene family, six full-length, intact putative tran-
scription factors were isolated from G. hirsutum
(GhNAC1-GhNAC6) that showed differential gene re-
gulation under dehydration, high salt, cold and ABA
Copyright © 2013 SciRes. OPEN ACCESS
M. Zahur et al. / Advances in Bioscience and Biotechnology 4 (2013) 15-20 17
4. HD-ZIP PROTEINS
HDZip proteins are characterized by the presence of a
DNA-binding homeodomain (about 60 amino acid long)
with a closely linked leucine zipper motif functioning in
dimer formation . The leucine zipper motif adjoining
to the C-terminal of the homeodomain is assumed to
form an amphipathic α-helix with a series of leucine re-
sidues responsible for dimerization of a pair of target
DNA contacting surfaces . Leucine zippers are re-
sponsible for the interaction of HD-Zip proteins among
each other and with other leucine zipper proteins .
Homo- and heterodimer interactions may have important
role in the function of these proteins . This type of
homeodomain association is present only in plants and it
is considered that HD-Zip genes originated in plant line-
age by exon exchange between a homeodomain gene and
a leucine zipper containing sequence . None of the
nearly 350 homeobox genes examined in animal system
contains a leucine zipper .
So far, the homeodomain-leucine zipper proteins have
been identified in many plants such as sunflower [32,33],
carrot , soybean , tomato , rice  and Ara-
bidopsis . These proteins have been suggested as ex-
cellent candidates to activate developmental responses to
altering environmental conditions, a characteristic fea-
ture of plants. Numerous authors have suggested that ex-
pression of HD-Zip transcription factors family is regu-
lated by diverse external factors such as illumination or
drought. HD-Zip proteins are categorized into four class-
es (I - IV) based on gene structure, presence of unique
domains and function . A few HDZip family mem-
bers are supposed to control the development of particu-
lar plant regions, such as the vascular system is controll-
ed by (ATHB8, class III, ; Oshox1, class II,  Va-
hox1, class I, , and root hairs and trichomes
(ATHB10, class IV, .
The Arabidopsis genes Athb2 and Athb4 (both class II)
are highly induced by far-red light, indicating a role in
the shade avoidance response ; Athb6, Athb7 and
Athb12 are inducible by drought as well as ABA, imply-
ing their putative function in dehydration responses [44,
45]. From C. plantagineum, two HDZipgenes (CPHB-1
and CPHB-2, class II) are dehydration-inducible, and one
of them is ABA-inducible (CPHB-2) . Therefore,
they are thought to be involved in regulation of dehydra-
tion responses through different branches of the dehydra-
tion-induced signalling network, ABA-independent or
ABA-dependent. Similar overexpression was observed in
five families of Craterostigma plantagineum homeobox
leucine zipper genes (CPHB) that were isolated by Deng
et al. . All families of CPHB genes modulate their
expression against dehydration in leaves and roots. Aka-
shi et al.  isolated an HD-Zip gene from Wild water-
melon (Citrullus lanatus sp.) differentially expressed un-
der drought stress. Expression and functional studies on
the sunflower Hd-Zip II subfamily with special emphasis
on Hahb-10 from sunflower indicated that the members
are expressed primarily in mature photosynthetic tissues,
and up-regulated by etiolation and gibberellins in seed-
In vitro and in vivo binding assays have demonstrated
that HDZip proteins from Arabidopsis, C. plantagineum,
sunflower and rice preferentially bind to two 9-bp pseu-
dopalindromic sequences, CAAT (A/T) ATTG (HDE1)
and CAAT(G/C)ATTG (HDE2) . A few other bind-
ing sequences relevant to homeodomain proteins were
reported in plants like: A soyabean homeodomain leucine
zipper proteins bind to CATTAATTAG sequence present
in the phosphate response domain of VspB promoter 
and ATHB6 of plant-specific HD-Zip class targets the
core motif (CAATTATTA) present in its own promoter
that mediated ABA-dependent gene expression . With
the help of cis-acting elements, efforts to identify target
genes in planta will contribute greatly to the understand-
ing of HDZip function.
This is important to provide fundamental molecular in-
formation towards understanding of the biological roles
of the HD-Zip proteins in cotton and present a valuable
source for improving cotton varieties with resistance to
5. COTTON HD-ZIP PROTEINS
A number of homeodomain leucine zipper protein of dif-
ferent classes have been identified in different species of
cotton such as GbHB1 from G. barbadense and GaHOX1
and GaHOX2 from G. arboreum that plays a role in fiber
development  whereas G. hirsutum GhHB1 is involv-
ed in root development and salt stress . G. arboreum
GaHDZ protein was identified as ABRE binding protein.
It showed enhanced expression under salt, heavy metals
and drought treatments (Author unpublished data). Re-
cently three HD-Zip proteins designated as GhHB2,
GhHB3 and GhHB4 were isolated from cotton cDNA
library. All these proteins are suggested to be involved in
early seedling development whereas expression of these
Hb proteins was up-regulated in response to gibberellin
signaling . Another HD-Zipn IV family transcription
factor, Meristem Layer 1 (GbML1) was isolated and cha-
racterized from G. barbadense that interacted with a key
regulator of cotton fiber development. When expressed
in Arabidopsis, GbML1 increased the number of tri-
chomes on stems and leaves and increased the accumula-
tion of anthocyanin in leaves . L1 layer-speciﬁc HD-
ZIP gene from tetraploid G. hirsutum GhHD-1 is express-
ed in trichomes and early ﬁbres thus might play a role in
cotton ﬁbre initiation. Further microarray analysis of
Copyright © 2013 SciRes. OPEN ACCESS
M. Zahur et al. / Advances in Bioscience and Biotechnology 4 (2013) 15-20
GhHD-1 lines indicated that it potentially regulates the
levels of ethylene and reactive oxidation species (ROS)
through a WRKY transcription factor and calcium-sig-
nalling pathway genes to activate downstream genes ne-
cessary for cell expansion and elongation .
Plants respond and adapt to environmental stresses through
not only physiological and biochemical processes but
also molecular and cellular processes. Several genes with
various functions are induced by drought and cold stress-
es, and those various transcription factors are involved in
the regulation of these stress-inducible genes through
their specific binding to the cis-acting elements of their
promoters. Gaining an understanding of the mechanisms
that regulate the expression of these genes is a funda-
mental issue in plant biology and will be necessary for
the genetic improvement of plants cultivated in extreme
environments. There have been extensive studies regard-
ing the role of transcription and its regulation by promo-
ter elements during abiotic stress. Cotton is best known
for its fiber development but it suffers badly due to abi-
otic stresses. Several transcription factors have been re-
ported that confer resistance to cotton is against these
stresses. In the last decade HD-Zip proteins have been
found in different resistant varieties that could not only
support the cotton plants to withstand stress period but
also specifically involved in efficient fiber development.
These characteristics made the HD-Zip proteins an effi-
cient target for cotton genetic engineering to develop bet-
 Breshears, D.D., Cobb, N.S., Rich, P.M., Price, K.P.,
Allen, C.D., Balice, R.G., Romme, W.H., Kastens, J.H.,
Floyd, M.L., Belnap, J., Anderson, J.J., Myers, O.B. and
Meyer, C.W. (2005) Regional vegetation die-off in re-
sponse to global-change-type drought. Proceedings of the
National Academy of Sciences of the United States of
America, 102, 15144-15148.
 Schroter, D., Cramer, W., Leemans, R., Prentice, I.C.,
Araujo, M.B., Arnell, N.W., Bondeau, A., Bugmann, H.,
Carter, T.R., Gracia, C.A., de la Vega-Leinert, A.C., Er-
hard, M., Ewert, F., Glendining, M., House, J.I., Kanka-
anpaa, S., Klein, R.J., Lavorel, S., Lindner, M., Metzger,
M.J., Meyer, J., Mitchell, T.D., Reginster, I., Rounsevell,
M., Sabate, S., Sitch, S., Smith, B., Smith, J., Smith, P.,
Sykes, M.T., Thonicke, K., Thuiller, W., Tuck, G., Zae-
hle, S. and Zierl, B. (2005) Ecosystem service supply and
vulnerability to global change in Europe. Science, 310,
 Bray, E.A., Bailey-Serres, J. and Weretilnyk, E. (2000)
Responses to abiotic stress. Biochemistry & molecular bi-
ology of plants. In: Gruissem, W. and Jones, R., Eds.,
American Society of Plant Physiologists, Rockville,
 Knight, H. and Knight, M.R. (2001) Abiotic stress signal-
ling pathways: Specificity and cross-talk. Trends Plant
Science, 6, 262-267.
 Zhu, J.K. (2002) Salt and drought stress signal transduc-
tion in plants. Annual Review of Plant Biology, 53, 247-
 Shinozaki, K. and Yamaguchi-Shinozaki, K. (2007) Gene
networks involved in drought stress response and toler-
ance. Journal of Experimental Botany, 58, 221-227.
 Lenka, S.K., Lohia, B., Kumar, A., Chinnusamy, V. and
Bansal, K.C. (2009) Genome-wide targeted prediction of
ABA responsive genes in rice based on over-represented
cis-motif in co-expressed genes. Plant Molecular Biology,
 Chachar, Q.I., Solangi, A.G. and Verhoef, A. (2008) In-
fluence of sodium chloride on seed germination and seed-
ling root growth of cotton (Gossypium hirsutum L.). Pa-
kistan Journal of Botany, 40, 183-197.
 Szabolcs, I. (1994) The concept of soil resilience. Soil re-
silience and sustainable land use. In: Greenland, D.J. and
Szabolcs, I., Eds., CAB International and Willingford,
 Sakhanokho, H., Zipf, A., Rajasekaran, K., Saha, S., Shar-
ma, G. and Chee, P. (2004) Somatic embryo initiation and
germination in diploid cotton (Gossypium arboreum L.).
In Vitro Cellular & Developmental Biology—Plant, 40,
 Liu, D., Guo, X., Lin, Z., Nie, Y. and Zhang, X. (2006)
Genetic Diversity of Asian Cotton (Gossypium arboreum
L.) in China Evaluated by Microsatellite Analysis. Gene-
tic Resources and Crop Evolution, 53, 1145-1152.
 Feng, C. and Stewart, J.M. (2003) A cdna-AFLP profile
of cotton genes in Response to Drought Stress. AAES Re-
search Services, 176-182.
 Heming, E., Sanden, A. and Kiss, Z.H. (2010) Designing
a somatosensory neural prosthesis: Percepts evoked by
different patterns of thalamic stimulation. Journal of Neu-
ral Engineering, 7, 064001.
 Wang, W., Vinocur, B. and Altman, A. (2003) Plant re-
sponses to drought, salinity and extreme temperatures:
Towards genetic engineering for stress tolerance. Planta,
218, 1-14. http://dx.doi.org/10.1007/s00425-003-1105-5
 Xu, Y.H., Wang, J.W., Wang, S., Wang, J.Y. and Chen,
X.Y. (2004) Characterization of GaWRKY1, a cotton
transcription factor that regulates the sesquiterpene syn-
thase gene (+)-delta-cadinene synthase-A. Plant Physiol-
ogy, 135, 507-515.
 Duan, H., Li, F., Wu, X., Ma, D., Wang, M. and Hou, Y.
Copyright © 2013 SciRes. OPEN ACCESS
M. Zahur et al. / Advances in Bioscience and Biotechnology 4 (2013) 15-20 19
(2006) Cloning and characterization of two EREBP tran-
scription factors from cotton (Gossypium hirsutum L.).
Biochemistry (Mosc.), 71, 285-293.
 Huang, B., Jin, L. and Liu, J.Y. (2008) Identification and
characterization of the novel gene GhDBP2 encoding a
DRE-binding protein from cotton (Gossypium hirsutum).
Journal of Plant Physiology, 165, 214-223.
 Meng, C., Cai, C., Zhang, T. and Guo, W. (2009) Charac-
terization of six novel NAC genes and their responses to
abiotic stresses in Gossypium hirsutum L. Plant Science,
 Ni, Y., Wang, X., Li, D., Wu, Y., Xu, W. and Li, X. (2008)
Novel cotton homeobox gene and its expression profiling
in root development and in response to stresses and phy-
tohormones. Acta Biochimica et Biophysica Sinica (Shang-
hai), 40, 78-84.
 Latchman, D.S. (1997) Transcription factors: An over-
view. The International Journal of Biochemistry & Cell
Biology, 29, 1305-1312.
 Pastori, G.M. and Foyer, C.H. (2002) Common compo-
nents, networks, and pathways of cross-tolerance to stress.
The central role of “redox” and abscisic acid-mediated
controls. Plant Physiology, 129, 460-468.
 Hartmann, U., Sagasser, M., Mehrtens, F., Stracke, R., and
Weisshaar, B. (2005) Differential combinatorial interac-
tions of cis-acting elements recognized by R2R3-MYB,
BZIP, and BHLH factors control light-responsive and tis-
sue-specific activation of phenylpropanoid biosynthesis
genes. Plant Molecular Biology, 57, 155-171.
 Hakimi, M.A., Privat, I., Valay, J.G. and Lerbs-Mache, S.
(2000) Evolutionary conservation of C-terminal domains
of primary sigma(70)-type transcription factors between
plants and bacteria. The Journal of Biological Chemistry,
 Nakashima, K., Ito, Y. and Yamaguchi-Shinozaki, K.
(2009) Transcriptional regulatory networks in response to
abiotic stresses in Arabidopsis and grasses. Plant Physi-
ology, 149, 88-95.
 Gao, S.Q., Chen, M., Xia, L.Q., Xiu, H.J., Xu, Z.S., Li,
L.C., Zhao, C.P., Cheng, X.G. and Ma, Y.Z. (2009) A cot-
ton (Gossypium hirsutum) DRE-binding transcription fac-
tor gene, GhDREB, confers enhanced tolerance to drought,
high salt, and freezing stresses in transgenic wheat. Plant
Cell Reports, 28, 301-311.
 Elhiti, M. and Stasolla, C. (2009) Structure and function
of homodomain-leucine zipper (HD-Zip) proteins. Plant
Signaling & Behavior, 4, 86-88.
 Lee, Y.H. and Chun, J.Y. (1998) A new homeodomain-
leucine zipper gene from Arabidopsis thaliana induced by
water stress and abscisic acid treatment. Plant Molecular
Biology, 37, 377-384.
 Landschulz, W.H., Johnson, P.F. and McKnight, S.L.
(1988) The leucine zipper: A hypothetical structure com-
mon to a new class of DNA binding proteins. Science,
 Schena, M. and Davis, R.W. (1994) Structure of homeo-
box-leucine zipper genes suggests a model for the evolu-
tion of gene families. Proceedings of the National Acade-
my of Sciences of the USA, 91, 8393-8397.
 Schena, M. and Davis, R.W. (1992) HD-Zip proteins: Mem-
bers of an Arabidopsis homeodomain protein superfamily.
Proceedings of the National Academy of Sciences of the
USA, 89, 3894-3898.
 Carabelli, M., Sessa, G., Baima, S., Morelli, G. and Ru-
berti, I. (1993) The Arabidopsis Athb-2 and -4 genes are
strongly induced by far-red-rich light. Plant Journal, 4,
 Chan, R.L. and Gonzalez, D.H. (1994) A cDNA encoding
an HD-zip protein from sunflower. Plant Physiology, 106,
 Gago, G.M., Almoguera, C., Jordano, J., Gonzalez, D.H.
and Chan, R.L. (2002) Hahb-4, a homeobox-leucine zip-
per gene potentially involved in abscisic acid-dependent
responses to water stress in sunflower. Plant, Cell & En-
vironment, 25, 633-640.
 Kawahara, R., Komamine, A. and Fukuda, H. (1995) Iso-
lation and characterization of homeobox-containing genes
of carrot. Plant Molecular Biology, 27, 155-164.
 Moon, Y.H., Choi, S.B., Kim, J.I., Han, T.J., Cho, S.H.,
Kim, W.T. and Lee, K.W. (1996) Isolation and Characte-
rization of a Homeodomain-leucine Zipper Gene, Gmh1,
from Soybean Somatic Embryo. Molecular Cells, 6, 366-
 Meissner, R. and Theres, K. (1995) Isolation and charac-
terization of the tomato homeobox gene THOM1. Planta,
195, 541-547. http://dx.doi.org/10.1007/BF00195713
 Meijer, A.H., Scarpella, E., van Dijk, E.L., Qin, L., Taal,
A.J., Rueb, S., Harrington, S.E., McCouch, S.R., Schil-
peroort, R.A. and Hoge, J.H. (1997) Transcriptional re-
pression by Oshox1, a novel homeodomain leucine zipper
protein from rice. The Plant Journal, 11, 263-276.
 Mattsson, J., Soderman, E., Svenson, M., Borkird, C. and
Engstrom, P. (1992) A new homeobox-leucine zipper
gene from Arabidopsis thaliana. Plant Molecular Biology,
18, 1019-1022. http://dx.doi.org/10.1007/BF00019223
 Ariel, F.D., Manavella, P.A., Dezar, C.A. and Chan, R.L.
(2007) The true story of the HD-Zip family. Trends in
Plant Science, 12, 419-426.
 Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I.
Copyright © 2013 SciRes. OPEN ACCESS
M. Zahur et al. / Advances in Bioscience and Biotechnology 4 (2013) 15-20
Copyright © 2013 SciRes.
and Morelli, G. (1995) The expression of the Athb-8 ho-
meobox gene is restricted to provascular cells in Arabi-
dopsis thaliana. Development, 121, 4171-4182.
 Scarpella, E., Rueb, S., Boot, K.J., Hoge, J.H. and Meijer,
A.H. (2000) A role for the rice homeobox gene Oshox1
in provascular cell fate commitment. Development, 127,
 Tornero, P., Conejero, V. and Vera, P. (1996) Phloem-
specific expression of a plant homeobox gene during
secondary phases of vascular development. The Plant
Journal, 9, 639-648.
 Di, C.M., Sessa, G., Dolan, L., Linstead, P., Baima, S.,
Ruberti, I. and Morelli, G. (1996) The Arabidopsis
Athb-10 (GLABRA2) is an HD-Zip protein required for
regulation of root hair development. The Plant Journal,
 Soderman, K., Werner, S., Pietila, T., Engstrom, B. and
Alfredson, H. (2000) Balance board training: Prevention
of traumatic injuries of the lower extremities in female
soccer players. A prospective randomized intervention
study. Knee Surgery, Sports Traumatology, Arthroscopy,
 Soderman, E., Hjellstrom, M., Fahleson, J. and Engstrom,
P. (1999) The HD-Zip gene ATHB6 in Arabidopsis is
expressed in developing leaves, roots and carpels and
up-regulated by water deficit conditions. Plant Molecular
Biology, 40, 1073-1083.
 Frank, W., Phillips, J., Salamini, F. and Bartels, D. (1998)
Two dehydration-inducible transcripts from the resurrec-
tion plant Craterostigma plantagineum encode interacting
homeodomain-leucine zipper proteins. The Plant Journal,
 Deng, X., Phillips, J., Meijer, A.H., Salamini, F. and
Bartels, D. (2002) Characterization of five novel dehy-
dration-responsive homeodomain leucine zipper genes
from the resurrection plant Craterostigma plantagineum.
Plant Molecular Biology, 49, 601-610.
 Akashi, K., Nishimura, N., Ishida, Y. and Yokota, A.
(2004) Potent hydroxyl radical-scavenging activity of
drought-induced type-2 metallothionein in wild water-
melon. Biochemical and Biophysical Research Commu-
nications, 323, 72-78.
 Tron, A.E., Bertoncini, C.W., Chan, R.L. and Gonzalez,
D.H. (2002) Redox regulation of plant homeodomain
transcription factors. The Journal of Biological Chemistry,
 Deng, X., Phillips, J., Brautigam, A., Engstrom, P., Jo-
hannesson, H., Ouwerkerk, P.B., Ruberti, I., Salinas, J.,
Vera, P., Iannacone, R., Meijer, A.H. and Bartels, D.
(2006) A homeodomain leucine zipper gene from Cra-
terostigma plantagineum regulates abscisic acid respon-
sive gene expression and physiological responses. Plant
Molecular Biology, 61, 469-489.
 Tang, Z., Sadka, A., Morishige, D.T. and Mullet, J.E.
(2001) Homeodomain leucine zipper proteins bind to the
phosphate response domain of the soybean VspB tripar-
tite promoter. Plant Physiology, 125, 797-809.
 Himmelbach, A., Hoffmann, T., Leube, M., Hohener, B.
and Grill, E. (2002) Homeodomain protein ATHB6 is a
target of the protein phosphatase ABI1 and regulates
hormone responses in Arabidopsis. The EMBO Journal,
21, 3029-3038. http://dx.doi.org/10.1093/emboj/cdf316
 Guan, X.Y., Li, Q.J., Shan, C.M., Wang, S., Mao, Y.B.,
Wang, L.J. and Chen, X.Y. (2008) The HD-Zip IV gene
GaHOX1 from cotton is a functional homologue of the
Arabidopsis GLABRA2. Physiologia Plantarum, 134,
 Qin, Y.F., Li, D.D., Wu, Y.J., Liu, Z.H., Zhang, J., Zheng,
Y. and Li, X.B. (2010) Three cotton homeobox genes are
preferentially expressed during early seedling develop-
ment and in response to phytohormone signaling. Plant
Cell Reports, 29, 1147-1156.
 Zhang, L., Xiao, S., Li, W., Feng, W., Li, J., Wu, Z., Gao,
X., Liu, F. and Shao, M. (2011) Overexpression of a
Harpin-encoding gene hrf1 in rice enhances drought tole-
rance. Journal of Experimental Botany, 62, 4229-4238.
 Walford, S.A., Wu, Y., Llewellyn, D.J. and Dennis, E.S.
(2012) Epidermal cell differentiation in cotton mediated
by the homeodomain leucine zipper gene, GhHD-1. The
Plant Journal, 71, 464-478.