全 文 ：Received 4 Nov. 2003 Accepted 2 Apr. 2004
Supported by the Hi-Tech Research and Development (863) Program of China (2001AA225031) and the National Natural Science Foundation
of China (90208009).
* Both authors contributed equally to this work.
** Author for correspondence. Tel: +86 (0)21 62431551; E-mail: .
*** Author for correspondence. Tel: +86 (0)21 64042090; E-mail: .
http://www.chineseplantscience.com
Acta Botanica Sinica
植 物 学 报 2004, 46 (7): 846-853
Characterizations of the uro Mutant Suggest that the URO Gene Is
Involved in the Auxin Action in Arabidopsis
GUO Ying-Li1, 2*, YUAN Zheng1*, SUN Yue1, 3**, LIU Jing2, HUANG Hai1***
(1. State Key Laboratory of Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes
for Biological Sciences, The Chinese Academy of Sciences, Shanghai 200032, China;
2. School of Life Sciences, University of Science and Technology of China, Hefei 230027, China;
3. College of Life Sciences, East China Normal University, Shanghai 200062, China)
Abstract: The Arabidopsis gene UPRIGHT ROSETTE (URO) was previously identified as a leaf develop-
mental regulator, as all rosette leaves of the semi-dominant upright rosette (uro) mutant grow uprightly at
seedling stages. Here, we report more detailed phenotypic characterizations of the uro mutant and show
that the URO gene has multiple functions in plant development. In addition to its aberrant leaf-growing
pattern, the uro mutant displayed pleiotropic phenotypes. Both uro/+ and uro/uro plants showed a loss of
apical dominance, while such a phenotype in the uro/uro plants appeared more severe. Some secondary
branches of the uro/uro plants were replaced by leaves, for which petioles were attached to the abaxial
side of leaves. Flowers often exhibited varying abnormalities, with altered numbers of petals and stamens
and abnormally fused organs. Stems of the uro mutant were soft, which was caused by lacking interfas-
cicular fiber. In addition, vascular differentiation in mutant stem was delayed. The loss of apical dominance
and the defects in vascular development and interfascicular fiber formation suggest that the URO function
might be associated with auxin-mediated plant development. To provide more direct evidence whether the
URO is involved in auxin action, we examined the URO function in auxin polar transportation pathway by
analyzing pinformed1 (pin1) uro double mutant. Phenotypes of the double mutant suggest that URO and
PINFORMED1 (PIN1) have partial genetic interactions in plant development, which further supports the
hypothesis that the URO gene may play an important role in the auxin regulatory pathway.
Key words: Arabidopsis ; auxin; interfascicular fiber; pinformed1; upright rosette
The plant hormone auxin plays a critical role in the regu-
lation of plant growth and development, including cell divi-
sion and expansion, vascular tissue differentiation, root
initiation, apical dominance, gravitropic and phototropic
responses, fruit ripening, leaf senescence, and abscission
of leaves and fruits (Eckardt, 2001). In recent years, our
understanding of auxin action in several research fields
has been advanced, especially in the auxin polar transport,
auxin metabolism, molecular basis of gene responses to the
auxin, and auxin-directed protein degradation. In particular,
many genes that function in the auxin-related regulatory
pathways have been uncovered mainly by studies of auxin-
defective mutants, and the functional characterizations of
these genes provide new insights into the plant develop-
ment (Kepinski and Leyser, 2002; Muday, 2002; Vogler and
Kuhlemeier, 2003). It is widely expected that the forward
genetic approach will be very useful in the future in dis-
secting auxin regulatory pathways by analyzing more novel
relevant mutants.
We reported in our previous work the identification of
several Arabidopsis mutants that are defective in leaf de-
velopment (Sun et al., 2000). One of these mutants, named
upright rosette (uro) that was isolated from the T-DNA-
insertional mutagenesis population, demonstrated abnor-
mal leaf growth pattern. Each rosette leaf at seedling stages
had a smaller angle to the primary inflorescence stem than
that in the wild-type leaves. Genetic analysis demonstrated
that the uro phenotype was caused by a semi-dominant
nuclear mutation, and the URO locus was mapped to the
short arm of chromosome 3, about 37 cM from telomere
(Sun et al., 2000). We report in this work the more detailed
phenotypic characterizations of the uro mutant. In addi-
tion to the abnormal leaf growth, the uro mutation results
in pleiotropic defects in the development of stem,
GUO Ying-Li et al.: Characterizations of the uro Mutant Suggest that the URO Gene Is Involved in the Auxin Action in
Arabidopsis 847
inflorescence, floral organs and fruit. The loss of apical
dominance and the abnormality in interfascicular fiber in
the uro mutant strongly suggest that the URO gene may
play an important role in auxin action.
1 Materials and Methods
1.1 Plant materials and growth conditions
Arabidopsis semi-dominant mutant uro, which is in the
Landsberg erecta (Ler) genetic background, was obtained
in our previous work from a T-DNA mutagenesis experi-
ment (Sun et al., 2000). The uro mutant has been back-
crossed to the wild-type Ler three times before the pheno-
typic characterizations. The pinformed1 (pin1) mutant was
from Klaus Palme (Max-Planck-Gesellschaft, Koln,
Germany). Plants were grown in soil according to our pre-
vious conditions (Chen et al., 2000).
1.2 Double mutant construction
Double mutant pin1 uro was constructed by a cross
between homozygous uro and heterozygous pin1 plants,
and the F1 plants that showed uro phenotypes were selfed.
F2 segregation data were close to a 9:3:3:1 ratio. In total 470
F2 plants, the distribution was 260 uro, 88 wild type, 87 uro
pin1 that showed a novel plant stature and flower
phenotypes, and 35 pin1.
1.3 Histology
Fresh tissues and organs from wild-type and mutant
plants were examined under a SZH10 dissecting microscope
(Olympus, Japan), and photographed using a Nikon E995
digital camera (Nikon, Japan). Hand sectioning of inflores-
cence stem was performed using a razor blade to generate
thin sections of live material. For anatomical observation,
sections were stained with 0.02% toluidine blue for 2 min,
and then rinsed with water. Sections were viewed with a
Zeiss light microscope (Zeiss, Germany) using bright-field
illumination.
1.4 Scanning electron microscopy
Fresh flowers and inflorescences were fixed with FAA
at room temperature overnight, and then dehydrated through
a graded alcohol series of 70%, 85%, 95% and 100% of
ethanol, followed by a change to 100% ethanol once, each
for 5 min. The specimens were then critical point-dried
using liquid carbon dioxide, and mounted on scanning elec-
tron microscopy (SEM) stubs. The mounted specimens
were sputter-coated with gold and palladdium (4:1) and ex-
amined with a scanning electron microscope (Hitachi S-
2460, Japan).
2 Results
2.1 Mutant effects on the plant architecture
In contrast to the wild-type Arabidopsis plant (Fig.1A),
the heterozygous uro mutant (uro/+) plant was shorter in
stature with reduced apical dominance (Fig.1B). Mature
wild-type plants usually have a long primary inflorescence
stem with a few shorter branches arising from different parts
of the primary stem (Fig.1A). However, uro/+ plants did
not show such a predominant inflorescence stem, and most
branches arose from lower positions of the primary inflo-
rescence stem, very close to the rosettes (Fig.1B). The
homozygous uro plant (uro/uro) displayed similar plant
architecture to that of the uro/+ plant, but the phenotypes
appeared more severe (Fig.1C), with a very short plant
stature. In the wild-type, each branch on inflorescence
stem was associated with a cauline leaf, which grew at the
proximal end of the branch. Interestingly, in uro/uro plants,
branches were frequently converted to leaves, for which
petioles attached to the abaxial side of the lamina (Fig.1C,
arrowhead). We refer to this structure as the lotus-leaf.
Since it is usually thought that plant apical dominance is
regulated by auxin (Eckardt, 2001), the mutant architecture
suggests that the URO gene may be involved in the auxin
action.
2.2 Mutant effects on the plant vegetative development
During the seedling stages, all leaves except cotyledons
in both uro/+ and uro/uro plants were upright (Fig.1D,
right; for comparison, see a wild-type plant on the left).
Although leaves of both uro/+ and uro/uro mutants were
broader (Fig.1F,G) than that of the wild-type (Fig.1E), the
patterns of leaf venation kept unchanged. Stems of the uro
mutant were soft, and became thicker towards the basal
portion (Fig.1H). In the uro/uro plants, most secondary
branches were longer than the primary inflorescence stem
(Fig.1I). Phenotypic analyses in the uro vegetative growth
indicate that the URO gene has multiple functions in regu-
lation of plant development.
2.3 Mutant effects on the reproductive development
The uro mutation affected a number of processes in
plant reproductive development. First, the flowering time
was altered in the mutant plants. In comparison to the wild-
type plants, the uro/+ and uro/uro plants delayed in flow-
ering time (Fig.2). Second, although early appearing flow-
ers of the uro/+ and uro/uro looked normal, later flowers
showed varying aberrant phenotypes. These included
developmentally incomplete flowers, which frequently died
before seeds set (Fig.1J, arrowhead), altered petal numbers
(Fig.1K), asymmetrically arranged floral organs such as sta-
mens (data not shown) and petals (Fig.1L), and abnormally
fused carpels that were sterile (Fig.1M). Finally, mutant
plants formed siliques that were usually shorter than those
Acta Botanica Sinica 植物学报 Vol.46 No.7 2004848
in wild-type plants (Fig.1N), regardless of uro/+ (Fig.1O)
or uro/uro (Fig.1P) mutant plants. In addition, sepals, pet-
als and stamens often firmly attached to the silique on fruit
maturation (Fig.1O, P). The morphological observations of
the uro mutant reveal that the URO functions are involved
in the different developmental processes.
2.4 The uro mutant altered endodermis pattern and lacked
interfascicular fibers in stems
uro plants have very soft inflorescence stem as de-
scribed (see above). To investigate the defect at the
Fig.1. Phenotypes of upright rosette mutant. A-C. Plant morphology. A. A wild-type Landsberg erecta (Ler) plant. B. A uro/+ plant.
C. A uro/uro plant. Arrowhead shows that the uro/uro plants sometimes generate lotus-leaves. D. A wild-type (left) and a uro/uro
seedlings. All rosette leaves of the uro/uro mutant at the seedling stages grow uprightly. E-G. Comparison of rosette leaves. E. A Ler
rosette leaf. F. A uro/+ leaf. G. A uro/uro rosette leaf. From E to G, rosette leaves are broader in uro/+ and uro/uro mutants than those
in the Ler plants, but the venation patterns are similar between wild-type (E) and mutant leaves (F, G). H. A wild-type stem (left) and
a uro/+ stem (right), which becomes thicker towards the basal part. I. A primary inflorescence stem (arrowhead) and some secondary
inflorescence stems (arrows) in a uro/uro plant, showing that the primary inflorescence stem in the uro/uro plant is usually very short.
J. Some uro/uro flowers die before seeds set (arrowhead). K. A uro/uro flower with an increased petal. L. Later uro/uro flowers contain
asymmetrically arranged petals. M. Some later uro/uro flowers have increasingly fused carpels. N-P. Siliques of the wild-type and
mutants. The siliques in the Ler plants (N) are usually longer than those in the uro/+ (O) and uro/uro (P) mutants, and sepals, petals and
stamens in the mutants do not detach from siliques even when seeds are mature. Q. A section from the elongation part of a wild-type
primary stem. R. A close-up of (Q). S. A section from the elongation part of a uro/+ primary stem. T. A close-up of (S). From (Q) to
(T), the endoderm cells in the mutant are proliferated while interfascicular fiber diminishes in this region of the stem. U. A section from
basal part of a wild-type primary stem. V. A close-up of (U). W. A section from basal part of a uro/+ primary stem. X. A close-up of
(W). From (U) to (X), although interfascicular fibers appear in the basal part of the uro/+ mutant, the cell layers are much fewer than
those in the wild type. co, cortex; e, epidermis; en, endodermis; ph, phloem; pi, pith; if, interfascicular fiber; ip, interfascicular fiber
precursor; mx, metaxylem; x, xylem. A and B, bars = 1 cm; C and I, bars = 0.5 cm; from D to H and from J to M, bars = 0.1 cm; from N
to P, bars = 0.2 cm; Q, S, U, and W, bars = 100 mm; R, T, V, and X, bars = 50 mm.
GUO Ying-Li et al.: Characterizations of the uro Mutant Suggest that the URO Gene Is Involved in the Auxin Action in
Arabidopsis 849
cellular level, we analyzed cell types in uro stem by cross
sectioning. Fibers can be found in various parts of plants.
In stems of the wild-type plants, interfascicular fibers are
needed for support of the shoots. We first examined the
fiber formation in wild-type plants, and a lignin staining
reagent, toluidine blue, was used to show fiber distribution
in stems of 5-week-old plants. In the elongation part
(Fig.1Q, R) and the basal part (Fig.1U, V) of a wild-type
stem, blue staining was clearly seen in vascular bundles
and interfascicular fibers that are the arch-shaped cell lay-
ers between vascular tissues. In comparison, the blue
staining in elongation part of the uro/+ stem was only con-
centrated in xylem (Fig.1S, T). Although interfascicular fi-
ber precursors existed in the elongation part of the mutant
stem, further lignification of the fibers did not seem to be
processed. In the basal part of the uro/+ stem, blue stain-
ing was observed in interfascicular fibers as well as in xylem;
however, fiber cell layers in the mutant (Fig.1W, X) were
much fewer than those in the wild-type stem (Fig.1V).
Furthermore, the endodermis of the uro/+ (Fig.1S,T,W, X)
and the uro/uro (see below) stems were overly proliferated,
resulting in a thickened endoderm zone.
2.5 Early abnormalities in uro flower development
To better understand the URO regulation in flower
development, we analyzed early flowers of the uro mutants
by SEM. The wild-type Arabidopsis inflorescence usually
produces a continuous and indeterminate number of flower
primordia on its flanks (Okada et al., 1991). Even in the late
stages of plant development, emergence of new flower pri-
mordia was evident (Fig.3A, arrow). In the uro/+ mutant,
inflorescences at early developmental stages normally pro-
duced flower primordia, similar to that in the wild-type (Fig.
3B, arrow). However, at later stages, some uro/+ plants
gave rise to a terminal flower, which was chimeric with dif-
ferent floral organs (Fig.3C). uro/uro plants showed the
similar flower development pattern to the uro/+ plants,
whereas flower termination in the uro/uro plants appeared
even earlier (data not shown). In addition, some floral or-
gans in the uro/uro mutant displayed homeotic changes:
Fig.2. Flowering time of the wild-type and upright rosette
mutants. Flowering rates are given by the each-day flowering
number to divide the total flowers during the first 10 d after
flowering. Flowers after this period were not counted because
the flowering numbers were decreased to a very low level. The
first day for scoring flowers was at day 22 after seed germination,
when wild-type plants began to flower. A total of 138, 259 and
90 flowers in the first 10 d were analyzed for the wild-type,
uro/+ and uro/uro plants, respectively.
Fig.3. Scanning electron microscopy of wild-type and upright
rosette inflorescences and flowers. A. A wild-type inflorescence.
Arrow denotes a new flower primordium emerging from central
inflorescence. B. An early-stage uro/+ inflorescence, showing a
newly growing flower primordium (arrow). C. A late-stage uro/+
flower inflorescence, which forms terminal flowers with different
floral organs fused together. D. A uro/uro flower showing a
homeotic conversion with stigmatic papillae grown on a sepal.
Inflorescence and flower specimens were from 4-week-old plants.
Acta Botanica Sinica 植物学报 Vol.46 No.7 2004850
stigmatic tissues that usually topped the gynoecium ap-
peared on the tips of sepals (Fig.3D). The SEM results
indicate that the URO functions are required for flower ter-
mination and may be involved in the regulation of floral
homeotic genes.
2.6 Phenotypes of the pin1 uro double mutant
Phenotypes of the uro mutant such as the loss of apical
dominance and the block of interfascicular differentiation
are generally thought to be associated with the defective
auxin regulation (Zhong et al., 1997; Zhong and Ye, 2001;
Booker et al., 2003). Therefore, it is possible that the URO
function is involved in the auxin-regulated development.
Auxin regulation is a very complex physiological process,
which relates to several aspects that have been investi-
gated extensively: auxin synthesis and metabolism, auxin
polar transport, response of gene expression to auxin and
auxin-directed protein degradation. To examine whether
URO gene functions in one of these aspects in auxin action,
we first tested auxin polar transport by construction of uro
and pin-formed1 (pin1) double mutant.
PIN1 is a transmembrane protein involved in the auxin
efflux in auxin polar transport (Galweiler et al., 1998). Loss
of function in the PIN1 protein severely affects organ
initiation, and the pin1 mutation is characterized by an in-
florescence meristem that does not initiate any flower, re-
sulting in the formation of a naked inflorescence stem (Fig.
4A). Different to the pin1 single mutant, the pin1 uro/+
usually produced a few secondary inflorescences with a
cauline leaf at the proximal end of each branch (Fig.4B).
Although the pin1 uro/uro had a very short plant stature
(Fig.4C), similar to that of the uro/uro mutant (Fig.1C), sec-
ondary branch numbers were reduced significantly (26 in
20 pin1 uro/uro plants versus 67 in 20 uro/uro plants). A
novel inflorescence phenotype appeared in the pin1 uro/
uro double mutants, which was different from those in ei-
ther wild-type plant (Fig.4D) or its parents (Fig.4A, E, F).
The uro/+ inflorescence (Fig.4E) was quite similar to that
in the wild-type (Fig.4D) at the early flowering stage. The
inflorescence pattern of the uro/uro was also similar to that
of the wild-type, except that the mutant inflorescence was
terminal after producing a limited numbers of flowers (Fig.
4F). However, at the later flowering stages, the pin1 uro/+
double mutant usually generates flowers containing exag-
gerated stigmatic tissues, with a few petals and stamens
(Fig.4G). The pin1 uro/uro double mutant produced many
flowers. In addition to the abundant stigmatic tissues, flow-
ers of pin1 uro/uro double mutant (Fig.4H) also contained
many chimeric floral organs with more petals and stamens
than those in the pin1 uro/+ flowers (Fig.4G). This kind of
flower often died early and was completely sterile. The
cellular pattern in the pin1 uro/uro stem (Fig.4J) reflected
the additive phenotypes of both parents (Fig.4I, K), with
partially restored interfascicular fibers and thick
endodermis. Phenotypic analyses of the pin1 uro double
mutant suggest that URO and PIN1 have partially genetic
interaction in plant development.
3 Discussion
The plant hormone auxin is a crucial player in plant de-
velopment throughout the life cycle by directing basic de-
velopmental processes such as cell division, cell elonga-
tion and differentiation. Although recent studies have pro-
vided new insights into the molecular bases of auxin action,
many aspects of the auxin regulation remain to be
addressed. Therefore, characterizations of biological mu-
tations disrupting genes that are involved in the auxin-
mediated developmental processes would be of great
significance. After causal characterizations of the uro
mutant, we propose that the URO gene may be one of the
important regulators in auxin action for reasons.
First, uro mutant demonstrated pleiotropic plant
phenotypes, including uprightly growing leaves and the
lotus-leaf structure, the thick basal part of stems, terminal
inflorescence, organ-fused flowers and homeotic conver-
sion of floral organs. Several other auxin-related mutants
showed the similar phenomena, although the varying ab-
normalities appear in different parts of plants. For example,
the predominant phenotypes of Arabidopsis mutants pin1
and pinoid (pid) are that the apical meristems produce ro-
sette leaves and a flowering shoot, but the shoot is fre-
quently devoid of flowers. These auxin-defective mutants
also show other phenotypes such as abnormal cotyledons,
leaves, stems, and floral organs (Bennett et al., 1995). ettin
(ett, Sessions and Zambryski, 1995; Sessions et al., 1997)
and monopters (mp, Przemeck et al., 1996; Hardtke and
Berleth, 1998) are other two Arabidopsis mutants defective
in auxin signaling. Abnormalities of these two mutants
appear in different types of floral organs. Since auxin regu-
lates many developmental processes in plant, mutation of a
single gene that is involved in the auxin action could cause
multiple and totally developmentally unrelated phenotypes.
Second, several phenotypes in the uro mutant reflect
typical auxin defects in plant. In plant architecture, the api-
cal dominance, whereby the growing apical meristem sup-
presses the growth of axillary meristems, is mediated by
auxin, as first proposed by Thimann and Skoog (1933). The
uro mutant shows a clear loss of apical dominance with
markedly increased shoot branches, and the secondary
GUO Ying-Li et al.: Characterizations of the uro Mutant Suggest that the URO Gene Is Involved in the Auxin Action in
Arabidopsis 851
branches are often longer than the primary inflorescence
stem. It is generally thought that plant vascular differentia-
tion is regulated by auxin. Arabidopsis gene AXR1 medi-
ates auxin signal, and mutations in the AXR1 gene result in
increased branches, with the degree of branching correlat-
ing with the degree of insensitivity to auxin in the different
alleles (Timpte et al., 1995). Recent studies demonstrate
that the expression of AXR1 in xylem and interfascicular
sclerenchyma tissues is sufficient to restore wild-type shoot
branching (Booker et al., 2003). In the uro mutant, the
differentiation of the interfascicular fiber is markedly de-
layed or even completely aborted, resulting in very soft
stems. Furthermore, lotus-leaves (or cup-shaped rosette
leaves) are also thought to associate with auxin signal. It
was reported that the pin1 mutants frequently show the
cup-shaped leaves (Reinhardt et al., 2000). In the tobacco
and Brasscia rape tissue culture, the media containing auxin
polar transport inhibitors HFCA and TIBA resulted in the
formation of lotus-leaves from explants (Ni et al., 1999).
Similar to the pin1 mutants, the uro mutant produces the
lotus-leaves. Therefore, it is possible that these pheno-
types are resulted from the indirect effects of the auxin
regulation.
Third, polar auxin transport controls different develop-
mental processes in plant, including the formation of vas-
cular tissue. Mutations in the PIN1 gene eliminate polar
auxin transport in inflorescence stem (Galweiler et al., 1998),
leading to a series of abnormal plant phenotypes: altered
Fig.4. Phenotypes of double mutant between upright rostte and pin-formed1. A-C. Morphology of single and double mutants. A. A
pin1 mutant plant. B. A pin1 uro/+ plant. C. A pin1 uro/uro plant. D-H. Comparison of inflorescences of single and double mutants.
D. A wild-type Ler inflorescence. E. A uro/+ inflorescence. F. A uro/uro inflorescence. G. A pin1 uro/+ inflorescence. H. A pin1 uro/
uro inflorescence. In (G) and (H), inflorescences of the uro/+ and uro/uro double mutants produce terminal flowers that are composed
of many different floral organs fused together. I-K. Analysis of cellular patterns of the stem. I. A section from the pin1 stem, showing
abundant interfascicular fibers. J. A section from the pin1 uro/uro stem, showing the reduced interfascicular fiber layers in comparison
with that in the pin1 stem (I). K. A section from the uro/uro stem, which contains no interfascicular fibers. All sections were from stems
of 4-week-old plants at the similar positions. en, endodermis; if, interfascicular fiber; ip, interfascicular fiber precursor; ph, phloem; x,
xylem; and mx, metaxylem. From A to B, bars = 1 cm; from C to H, bars = 0.2 cm; and from I to K, bars = 50 mm.
Acta Botanica Sinica 植物学报 Vol.46 No.7 2004852
cotyledon shapes, aberrant vascular patterns in stem, sup-
pression of the organ outgrowth, and defect in the estab-
lishment of organ boundaries (Vernoux et al., 2000). These
abnormalities were not seen in the uro mutant throughout
the entire plant development. In the pin1 uro double mutant,
although most phenotypes are additive, the phenotypes in
the inflorescence are novel. These results strongly sug-
gest that URO and PIN1 have partially genetic interactions
in the regulation of plant development and the URO gene is
involved in the auxin regulation.
The uro mutant was from our T-DNA mutagenesis
population, and genetic analysis has revealed that a T-DNA
insertion is tightly linked to the uro phenotypes (data not
shown). The molecular mechanisms of URO actions and
more precise gene functions will be clarified with the gene
sequences being determined.
Acknowledgements: The authors would like to thank
Klaus Palme and Masahiko Furutani for providing pin1
seeds, XUE Hong-Wei for bring the pin1 seeds to this labo-
ratory for the experiment, MAO Jian for technical assis-
tance in SEM.
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