Plant Physiol. (1999) 120: 113-120
-Radiation Induces Leaf Trichome Formation in
Arabidopsis1
Toshifumi Nagata,
Setsuko Todoriki,
Toru Hayashi,
Yuriko Shibata,
Masaki Mori,
Hiromi Kanegae, and
Shoshi Kikuchi*
Japan Science and Technology Corporation, 2-1-2 Kannnon-dai,
Tsukuba Ibaraki 305-8602, Japan (T.N.); National Food Research
Institute, 2-1-2 Kannnon-dai, Tsukuba Ibaraki 305-8642, Japan (S.T.,
T.H.); University of Tsukuba, 1-1-1 Tennnou-dai, Tsukuba Ibaraki
305-8572, Japan (Y.S.); and National Institute of Agrobiological
Resources, 2-1-2 Kannnon-dai, Tsukuba Ibaraki 305-8602, Japan (M.M.,
H.K., S.K.)
 |
ABSTRACT |
We observed induction of additional
trichome formation on the adaxial surface of mature leaves of
Arabidopsis after massive doses (1-3 kilograys) of 
-radiation from
cobalt-60. A typical increase in trichome number was observed in the
seventh leaf when the full expansion of the fifth leaf was irradiated.
Under normal growth conditions, trichome numbers on the adaxial surface
of seventh leaf of the Arabidopsis ecotypes Columbia (Col) and
Landsberg erecta (Ler) were 122.5 ± 22.7 and 57.5 ± 14.5, respectively. However, -radiation
induced additional trichome formation and the numbers rose to
207.9 ± 43.7 and 95.0 ± 27.1 in Col and Ler, respectively. In Col the shape of new trichomes was intact and their
formation was spatially maintained at equal distances from other
trichomes. In Ler trichome morphology was aberrant and
the formation was relatively random. Treatment with antioxidants before -irradiation suppressed the increase in trichome number, and treatment with methyl viologen and light induced small trichomes. These
results suggest that -radiation-induced trichome formation is
mediated by active oxygen species generated by water radiolysis. -Radiation-induced trichome formation was blocked in the trichome mutants ttg-1, gl1-1, and
gl2-1. These results suggest that -radiation-induced trichome formation is mediated by the normal trichome developmental pathway.
| |
INTRODUCTION |
Massive doses of ionizing radiation have been shown to induce
physiological changes in plants, such as enhancement of respiration, increase in ethylene production (Young, 1965
; Abdel-Kader et al., 1968;
Lee et al., 1968; Akamine and Goo, 1971; Romani, 1984), induction of
enzyme activities (particularly for phenolic metabolisms; Riov et al.,
1970; Pendharkar and Nair, 1975; Frylink et al., 1987), and
accumulation of Suc (Hayashi and Aoki, 1985) and specific protein
species (Ferullo et al., 1994). Cellular macromolecular components such
as cell walls, membranes, and DNA are also markedly affected by
ionizing radiation (Casarett, 1968). These effects are considered a
consequence of both the direct interactions between the ionizing
radiation and the macromolecular structures and the indirect action of
AOS generated by water radiolysis.
We used Arabidopsis to elucidate the mechanisms of stress recognition,
signal transduction, and the initiation of plant self-protective programs at the molecular level because this plant provides certain key
advantages for genetic and molecular studies. We observed that
Arabidopsis displayed particular responses within several days after
irradiation with -rays (1-3 kGy) from cobalt-60 (1.17 and 1.33 MeV). These responses included accumulation of anthocyanin in the
aerial part of plant, induction of new trichome formation on the
adaxial surface of mature leaves, radial expansion of root cell layers,
and elongation of root hairs. In this paper we characterize -radiation-induced trichome formation.
Arabidopsis trichomes are single-cell-originated epidermal hairs that
serve as an appropriate model for plant cell differentiation and cell
elongation. The trichomes are present on the surfaces of the leaves,
stems, and sepals and on the margins of leaves and sepals. Plant growth
does not require trichomes, because plants that lack trichomes appear
to be fully viable and fertile (Koornneef et al., 1983). We have taken
a genetic approach to studying trichome development. More than 70 trichome mutants representing 21 different genes were isolated
(Lee-Chen and Steinitz-Sears, 1967; Feenstra, 1978; Koornneef et al.,
1982; Haughn and Somerville, 1988; Huelskamp et al., 1994; Marks and
Esch, 1994). Genetic and molecular biological studies have revealed
that the GL1 (GLABROUS1)
and TTG (TRANSPARENT TESTA
GLABROUS) genes are required for the initiation of
trichome development.
The GL1 gene has been cloned and shown to encode a putative
myb-class transcription factor (Oppenheimer et al., 1991;
Larkin et al., 1994b). GL1 transcripts are present at a low
level throughout the protoderm, with much higher levels of expression
in developing trichomes and presumptive trichome precursor cells
(Larkin et al., 1993). Mutations in TTG also affect
anthocyanin synthesis, integument development (Koornneef, 1981), and
root-hair patterning (Galway et al., 1994). The observation that
expression of the maize R gene in ttg mutant
plants complemented ttg mutation functionally (Lloyd et al., 1992) suggested that TTG encodes a homolog of
the maize R gene or the gene that regulates the expression
of an R homolog. However, recent cloning of the
TTG gene revealed no sequence homology to the
R gene (A.R. Walker and J.C. Gray, personal
communication).
The ectopic expression of GL1 with the cauliflower mosaic
virus 35S promoter does not lead to increased trichome formation, nor
does it bypass the requirement for TTG, whereas the ectopic expression of both GL1 and R induced an increase
in the trichome number (Larkin et al., 1994a). These results suggest
that the GL1 and TTG gene products cooperate in
promoting trichome initiation. The GL2 (GLABRA2)
gene is necessary for subsequent phases of trichome morphogenesis, such
as cell expansion, branching, and maturation of the trichome cell wall
(Koornneef et al., 1982; Marks and Esch, 1994; Rerie et al., 1994). The
GL2 gene has been also cloned and shown to have sequence
similarity to homeodomain proteins (Rerie et al., 1994). Detailed
expression analysis using anti-GL2 antibodies and the GUS
reporter gene fused to the GL2 promoter revealed that GL2 expression persists in mature trichomes. A requirement
of GL1 for GL2 expression in vivo has been
suggested (Szymanski et al., 1998). An examination of the distribution
of trichomes early in development disclosed that trichomes are
initiated adjacent to other trichomes much less frequently than would
be expected by chance.
Genetic and molecular biological studies have revealed the key genes
related to the developmental process of trichome formation and have
started the elucidation of the functions of these genes and their
interactions. However, stress-induced trichome formation has never been
found. In this paper we describe, for the first time to our knowledge,
the induction of new trichomes after -irradiation. We also examined
the conditions of new trichome formation thus induced and found that
the AOS generated by water radiolysis may also contribute to the
induction of new trichomes.
| |
MATERIALS AND METHODS |
Arabidopsis Strains and Growth Conditions
We used the wild-type Arabidopsis strains Columbia (Col) and
Landsberg erecta (Ler). The Arabidopsis Research
Center (Ohio State University, Columbus) provided the seeds of the
mutants gl1-1, gl1-2, gl2-1,
gl3-1, rhd2-1, and ttg-1. Sterilized
seeds were sown on 1% agar medium containing 1× Murashige and Skoog basal salts (Sigma), 2% Suc, 100 mg/L inositol, 1 mg/L thiamine, 0.5 mg/L nicotinic acid, and 0.5 mg/L pyridoxine and grown with 24 h
of continuous illumination (400-500 µW m
2
s1) at 21°C.
-Irradiation and Trichome Enumeration
Eighteen days after germination, when the fifth leaf had expanded
fully, the whole bodies of plants growing on agar medium were
irradiated with -rays from cobalt-60 using a -cell (3.0 kGy
h1, 1300 TBq; Nordion, Ontario, Canada). After
irradiation the plants grew alongside unirradiated plants in the same
conditions as before. Three days after irradiation, leaves were taken
from the plant and fixed in 4% paraformaldehyde and 2.5%
glutaraldehyde aqueous solution, pH 7.2 (Wako Chemicals, Richmond, VA)
at 4°C overnight. Water was substituted with 99.5% ethanol
for 4.5 h and then with 99% 2-methyl-2-propanol for 4 h
(both from Wako Chemicals). The leaves were then frozen at 
20°C for
30 min and dried for 8 h in a freeze dryer (model ES-2030,
Hitachi, Tokyo). Leaf trichomes were coated with an ion sputterer
(model E-1010, Hitachi) for 90 s. The trichomes were counted with
a scanning electron microscope.
| |
RESULTS |
-Radiation Induces Additional Trichome Formation
in Arabidopsis
Leaf trichomes occur mainly on the adaxial surface of the early
rosette leaves of Arabidopsis. Under our growth conditions (see
``Materials and Methods''), their number on the seventh leaf surface
was 122.5 ± 22.7 and 57.5 ± 14.5 in the control Col and
Ler, respectively. We found that massive doses (1-3 kGy) of
-radiation from cobalt-60 to Arabidopsis induced additional trichome
formation. The numbers of trichomes on the adaxial surface of sixth and
seventh leaves of unirradiated plants are distributed on the normal
probability curve (Fig. 1). When the
fifth leaf was fully expanded plants were irradiated at 2 kGy, and
3 d later the trichome numbers of the sixth and seventh leaves
were counted. As indicated in Figure 1, the peak trichome number
increased nearly 2-fold in both leaves of both ecotypes. However, there
were differences in the responses between the sixth and seventh leaves
and between ecotypes: The seventh leaf showed a clearer response than
the sixth leaf, and the increase in trichome number in Col was more
obvious than in Ler. Furthermore, no increase in trichome
number was observed in the first to fourth leaves, and the fifth leaf
showed a very small response (data not shown).
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| Figure 1.
Increase of trichome number after -radiation.
Trichome numbers on the adaxial surfaces of sixth and seventh leaves of
Col and Ler were counted and their distribution is
indicated in green. When the fifth leaf was fully expanded, about
18 d post germination, 2 kGy of -rays from cobalt-60 were
given. Three days later, the trichome numbers on the sixth and seventh
leaves were counted and their distribution is shown in red.
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These results suggest that the increase in trichome number is
dependent on the age of the leaf and on the ecotype. The timing of
radiation is very important to the ability of the epidermal cells to
differentiate into trichomes. We observed this difference between
ecotypes not only in the number of trichomes but also in the shape and
spatial distribution of new trichomes. Scanning electron microscope
images of trichomes are shown in Figure
2. In Col the spatial distribution and
shape of the trichomes maintained a similarity to those under normal
growth conditions during the process of trichome formation. However, in
Ler we saw abnormally branched trichomes and an aberrant
trichome similar to those observed in the Triptychon
mutant (Huelskamp et al., 1994). We also saw twinned trichomes and four
branched trichomes similar to those in the unirradiated Ler
shown in Figure 2, E and F (approximately 0.5% of normally
existing trichomes in Ler), indicating that the characteristics of trichomes in Ler developed successively
after -irradiation.
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| Figure 2.
Scanning electron micrographs of the leaf surface.
A, Adaxial surface of the seventh leaf of Col. Bar = 1 mm. B,
Adaxial surface of the seventh leaf of -radiated Col. Bar = 1 mm. C, Adaxial surface of seventh leaf of Ler. Bar = 1 mm. D, Adaxial surface of -radiated Ler. Bar = 1 mm. E, Trichome with aberrant branching observed on the adaxial
surface of -radiated Ler. Bar = 0.2 mm. F, Twin
trichome observed on the adaxial surface of -radiated
Ler. Bar = 0.2 mm.
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AOS Contribute to -Radiation-Induced Additional
Trichome Formation
To dissect the process of -radiation-induced trichome formation
physiologically, we examined the components contributing to the
induction process. At least two events may contribute to this process:
DNA damage and the generation of AOS such as hydroxide, superoxide, and
hydroxyl radicals. -Radiation is known to induce both genomic and
organellar DNA double-stranded breakage and to generate AOS through
water radiolysis. To determine whether AOS participate in
-radiation-induced trichome formation, we performed two types of
experiments: (a) treatment with an antioxidant (a radical scavenger)
before -irradiation, and (b) treatment with methyl viologen under
light. If the radicals generated by -radiation contributed to
-radiation-induced trichome formation, then antioxidant treatment
before -irradiation should suppress trichome formation. Likewise,
treatment with methyl viologen under light (which increases the
cytoplasmic concentration of superoxide radicals by trapping electrons
generated by PSI; Nakano and Asada, 1980) should induce new trichomes
to form on the leaf surfaces.
We used pyrrolidine dithiocarbamate, n-propyl gallate, and
nordihydroguaiaretic acid as antioxidants. One hundred microliters of
aqueous solution in three different concentrations was dropped into the
basal region of the plants once a day for 3 d before dosing them
with 2 kGy of -radiation. Three days after irradiation, trichomes
were counted; the results are shown in Table
I. Addition of an antioxidant without
-radiation did not cause a critical change in trichome number.
Although 1 mM of pyrrolidine dithiocarbamate could suppress
the increase of trichome number, 0.01 mM
nordihydroguaiaretic acid could not. A 10-fold increase (0.1 mM) of the acid completely suppressed it, however. We
obtained similar results with n-propyl gallate.
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Table I.
Average number of trichomes on the adaxial surface
of the seventh leaf following treatment with the antioxidants
pyrrolidine dithiocarbamate (PDTC), nordihydro-guaiaretic acid (NDGA),
and n-propyl gallate (n-PG) before -radiation
Data are means ± SE of 100 plants.
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One hundred milliliters of 2 µM methyl viologen was added
to the full expansion of the fifth leaf of experimental plants, and the
same volume of water was added to the control plants. The plants then
grew under light for 3 d, and we counted the trichomes on the
seventh leaf. As shown in Figure 3,
treatment with methyl viologen, but not with water, induced new but
small, branched, trichome-like hairs among the preexisting trichomes.
The surface of the methyl-viologen-treated leaf (Col) is shown in
Figure 3A and a magnified view appears as Figure 3B. Table
II shows the results of counting these
hairs. These data suggest that the number of preexisting mature-sized
trichomes did not change after the methyl-viologen treatment; however,
it was only after the treatment that we observed the small
trichome-like structures.
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| Figure 3.
Scanning electron micrographs of the leaf surface
of plant treated with methyl viologen. A, Adaxial surface of the
seventh leaf of Col treated with methyl viologen and grown for 3 d
under light. Small trichome-like hairs are indicated with "O."
Bar = 0.5 mm. B, Magnified view of A. Bar = 0.2 mm.
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Table II.
Average number of trichomes on the adaxial surface
of the seventh leaf 3 d after treatment with methyl viologen
Data are the means ± SE of 100 plants.
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These results indicate that treatment with antioxidants before
-irradiation suppresses additional trichome formation, and treatment
with methyl viologen induces trichome-like hair formation. Because
treatment with methyl viologen did not induce DNA damage, AOS, rather
than damaged DNA, must have contributed to the -radiation-induced trichome formation.
Genes Contributing to Normal Trichome Formation Also Contribute to
-Radiation-Induced Trichome Formation
Genetic analyses revealed that the GL1 and
TTG genes are required for the initiation of trichome
development. GL2 and GL3 genes are thought to be
the targets of GL1 and TTG genes. The trichome
phenotypes of gl2 and gl3 mutants are quite
similar: Mutants in both genes have fewer than normal trichomes and the trichomes are less branched than normal (Larkin et al., 1994b). Under
our growth conditions the root-hair-defective mutant rhd2-1 (Schiefelbein and Somerville, 1990) also exhibited a glabrous phenotype. To determine whether these genes are required for
-radiation-induced trichome formation, -radiation was given to
these mutants (Table III). The allele
gl1-1 has a deletion of the entire coding region (Oppenheimer et al., 1991). Additional trichome formation after -irradiation was completely suppressed. On the other hand,
gl1-2 is a relatively leaky allele, because only a few amino
acids in the C-terminal region are deleted from the GL1
protein (Esch et al., 1994). -Radiation given to this mutant induced
the increase of trichome number in the margin and the formation of new
trichomes on the surface; see Figure 4, A
and B.
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| Figure 4.
Scanning electron micrographs of the leaf
surface of trichome mutants treated with -radiation. A, Adaxial
surface of the seventh leaf of the gl1-2 mutant.
Bar = 1 mm. B, Adaxial surface of the seventh leaf of -radiated
gl1-2 mutant. Bar = 1 mm. C, Adaxial surface of the
seventh leaf of the gl2-1 mutant. Bar = 1 mm. D,
Adaxial surface of the seventh leaf of -radiated
gl2-1 mutant. Bar = 1 mm. E, Immaturely branched
trichome observed on the surface of leaf shown in D. Bar = 0.2 mm.
F, Adaxial surface of the gl3-mutant. Bar = 1 mm.
G, Adaxial surface of -radiated gl3-1 mutant.
Bar = 1 mm. H, New trichomes induced by -radiation of the
ttg-1 mutant. Bar = 1 mm. I, Immature trichome
induced by -radiation of the rhd2-1 mutant. Bar = 0.2 mm.
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|
The allele gl2-1 shows reduced trichome number and
less-branched trichomes (Fig. 4E). An increase of less-branched
trichomes was not clear after -radiation (Table III; Fig. 4, C and
D). Although gl3-1 showed a phenotype similar to
gl2-1, the number of less-branched trichomes in
gl3-1 increased after -radiation (Table III; Fig. 4, F
and G). A small number of trichomes existed along the margin of the
allele ttg-1, but -irradiation could not induce new
trichome formation (Table III; Fig. 4H). The rhd2-1 mutant
was hairless on the adaxial surface of leaves; however, -radiation
induced the formation of a few unbranched trichomes (Fig. 4I). These
results suggest that the GL1, TTG, and
GL2 genes are required not only for the normal
development of trichomes, but also for -radiation-induced trichome formation. The mutation of GL3 and RHD2
genes could not suppress -radiation-induced trichome formation.
| |
DISCUSSION |
We gave a massive dose of -radiation to Arabidopsis plants and
found that the number of leaf trichomes increased. This phenomenon was
typically observed on the adaxial surface of the seventh leaf after the
fifth leaf had fully expanded and the plant was then irradiated. The
response of the ecotypes Col and Ler were compared. Col
showed a much clearer response than Ler. This difference may be related to the difference in original trichome number in both ecotypes (Larkin et al., 1993). To elucidate which locus is
required for the response, crossing of both ecotypes and quantitative
trait analysis is necessary.
The fact that treatment with antioxidants before -radiation
suppressed trichome formation, whereas methyl viologen treatment under light induced it, suggests that -radiation-induced trichome formation is mediated by AOS. We are not sure whether normal
(developmental) trichome formation is also mediated by AOS. Different
SOD-like activities in Col and Ler revealed by electron spin
resonance analysis (data not shown) might explain the different
responses of these ecotypes to -radiation. Under normal growth
conditions the SOD-like activity in Ler is twice as high as
that in Col. If superoxide molecules were required for developmental
trichome formation, the difference in trichome number between the two
ecotypes might be due to the presence of SOD-like enzyme activity and
surviving superoxide molecules in leaves. To examine this possibility,
we are currently producing transgenic plants that express the SOD enzyme ectopically in Col to determine the relationship between the
expression of SOD activity and the leaf trichome number.
Leaf age is also important; we observed an increase in trichome
number in leaves that expanded after -irradiation but not in leaves
that had already expanded. This may have been due to the extinction of
the activator for trichome differentiation, aging of the leaf, or the
presence of an inhibitor to trichome differentiation in aged leaves. If
-radiation activates some genes required for trichome development,
in situ expression analysis of genes such as GL1 and
TTG may provide insight into the inducibility of trichome
formation. Scanning electron microscope observation revealed that new
trichomes developed not randomly but relatively equidistant to the
already present trichomes. In the normal development of leaf trichomes
a minimum distance between neighboring trichomes is maintained (Larkin
et al., 1993) and this pattern-formation rule is
maintained after -radiation.
-Irradiation of trichome mutants demonstrated that whereas the
GL1 and TTG gene products are required for
-radiation to induce trichomes, the GL3 and
RHD2 gene products are not, suggesting that the
GL3 gene product is required for at least two distinct functions: The phenotype of the gl3-1 mutation shows that
GL3 is required for the establishment of the full complement
of trichomes and for the branching of trichome cells. -Irradiation
of gl3-1 induced the formation of unbranched trichomes,
indicating that the maintenance of trichome number is suppressed by
-radiation and suggesting that GL2 and GL3
individually contribute to the development of trichomes.
Another interesting observation was that the mutation of the
RHD2 gene affected not only root hairs but also trichomes.
Although Schiefelbein and Somerville (1990) have reported that none of the root-hair mutations affect trichome morphology, under our experimental conditions the rhd2-1 mutation produced a
glabrous phenotype. It is possible that the same gene is required for
both root-hair differentiation and trichome development, because they are both single-cell-originated and stalk-differentiation processes. The phenotype of the rhd2-1 mutation after -irradiation
suggests that the functional defect of the rhd2-1 mutation
was partially bypassed.
Many trichome mutants have now been isolated and intensive genetic
studies have revealed the epistatic relationships of the genes and the
cascades of gene action. Some useful promoter and reporter gene
constructs were used to analyze the expression of the transcripts of
key regulatory genes such as GL1 and GL2. In addition to these molecular tools, the finding of -radiation-induced trichome formation should prove useful for the analysis of trichome development in Arabidopsis.
| |
FOOTNOTES |
1
This study was supported by a grant from the
Regional Links Research Program at Nagasaki of Japan Science and
Technology Corporation. It was also partially funded by the Ministry of
Agriculture, Forestry and Fisheries of Japan.
*
Corresponding author; e-mail skikuchi{at}abr.affrc.go.jp; fax
81-298-38-7007.
Received December 21, 1998;
accepted February 10, 1999.
| |
ABBREVIATIONS |
Abbreviations:
AOS, active oxygen species.
kGy, kilograys.
SOD, superoxide dismutase.
| |
ACKNOWLEDGMENTS |
The Arabidopsis mutants used in this work were
kindly provided by the Arabidopsis Biological Resource Center at Ohio
State University. We are grateful to Chieko Yoshida, Kazuko Yagi, Keiko Takahashi, Ikuko Hasegawa, Rie Abe, Kazuko Toyoshima, Yumiko Iguchi, and Keiko Takeuchi for assistance with experimental procedures. We also
thank Dr. Izumi Matsuda for providing important information about the
use of the scanning electron microscope.
| |
LITERATURE CITED |
Abdel-Kader AS,
Moris LL,
Maxie EC
(1968)
Physiological studies of gamma irradiated tomato fruits. I. Effects on respiratory rate, ethylene production and ripening.
Proc Am Soc Hortic Sci
92:
553-567
Akamine EK,
Goo T
(1971)
Respiration of gamma-irradiated fresh fruits.
J Food Sci
36:
1074-1077
Casarett AP
(1968)
Radiation chemistry and effects of gamma radiation on the cell.
In
AP Casarett,
eds, Radiation Biology.
Prentice-Hall, Englewood Cliffs, NJ
Esch JJ,
Oppenheimer DG,
Marks MD
(1994)
Characterization of a weak allele of the GL1 gene of Arabidopsis thaliana.
Plant Mol Biol
24:
203-207
[CrossRef][ISI][Medline]
Feenstra WJ
(1978)
Contiguity of linkage groups I and IV as revealed by linkage relationship of two newly isolated markers dis-1 and dis-2.
Arabidopsis Inf Serv
15:
35-38
Ferullo J-M,
Nespoulous L,
Triantaphylides C
(1994)
Gamma-ray-induced changes in the synthesis of tomato pericarp protein.
Plant Cell Environ
17:
901-911
Frylink L,
Dubery IA,
Schabort JC
(1987)
Biochemical changes involved in stress response and ripening behavior of gamma-irradiated mango fruit.
Phytochemistry
26:
681-686
Galway ME,
Masucci JD,
Lloyd AM,
Walbot V,
Davis RW,
Schiefelbein JW
(1994)
The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root.
Dev Biol
166:
740-754
[CrossRef][ISI][Medline]
Haughn GW,
Somerville CR
(1988)
Genetic control of morphogenesis in Arabidopsis.
Dev Genet
9:
73-89
Hayashi T,
Aoki S
(1985)
Effect of irradiation on the carbohydrate metabolism responsible for sucrose accumulation in potatoes.
J Agric Food Chem
33:
13-17
Huelskamp M,
Misera S,
Juergens G
(1994)
Genetic dissection of trichome cell development in Arabidopsis.
Cell
76:
555-566
[CrossRef][ISI][Medline]
Koornneef M
(1981)
The complex syndrome of ttg mutants.
Arabidopsis Inf Serv
18:
45-51
Koornneef M,
Dellaert SW,
van der Veen JH
(1982)
EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L) Heynh.
Mutat Res
93:
109-123
[ISI][Medline]
Koornneef M,
van Eden J,
Hanhart C,
Stam P,
Braaksma FJ,
Feenstra WJ
(1983)
Linkage map of Arabidopsis thaliana.
J Hered
74:
265-272
[Abstract/Free Full Text]
Larkin JC,
Oppenheimer DG,
Lloyd A,
Paparozzi ET,
Marks MD
(1994a)
The roles of GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development.
Plant Cell
6:
1065-1076
[Abstract]
Larkin JC,
Oppenheimer DG,
Marks DM
(1994b)
The GL1 gene and the trichome development pathway in Arabidopsis thaliana.
In
L Nover,
eds, Plant Transcription Factors.
Springer-Verlag, Berlin, pp 259-275
Larkin JC,
Oppenheimer DG,
Pollock S,
Marks MD
(1993)
Arabidopsis GLABROUS1 gene requires downstream sequences for function.
Plant Cell
5:
1739-1748
[Abstract]
Lee TH,
McGlasson WB,
Edwards RA
(1968)
Effect of gamma radiation on tomato fruit picked at four stages of development.
Radiat Bot
8:
259-267
Lee-Chen S,
Steinitz-Sears LM
(1967)
The location of linkage groups in Arabidopsis thaliana.
Can J Genet Cytol
9:
381-384
Lloyd AM,
Walbot V,
Davis RW
(1992)
Anthocyanin production in dicots activated by maize anthocyanin-specific regulators, R and C1.
Science
258:
1773-1775
[Abstract/Free Full Text]
Marks MD,
Esch JJ
(1994)
Morphology and development of mutant and wild type trichomes on the leaves of Arabidopsis thaliana.
In
J Bowman,
eds, Arabidopsis: An Atlas of Morphology and Development.
Springer-Verlag, New York, pp 56-73
Nakano Y,
Asada K
(1980)
Spinach chloroplast scavenge hydrogen peroxide on illumination.
Plant Cell Physiol
21:
1295-1307
[Abstract/Free Full Text]
Oppenheimer DG,
Hermann PL,
Sivakumarans S,
Esch J,
Marks MD
(1991)
A myb-related gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules.
Cell
67:
483-493
[CrossRef][ISI][Medline]
Pendharkar MB,
Nair PM
(1975)
Induction of phenylalanine ammonia-lyase (PAL) in gamma irradiated potatoes.
Radiat Bot
15:
191-197
Rerie WG,
Feldmann KA,
Marks MD
(1994)
The GLABRA2 gene encodes a homeodomain protein required for normal trichome development in Arabidopsis.
Genes Dev
8:
1388-1399
[Abstract/Free Full Text]
Riov J,
Monselise SP,
Kahan RS
(1970)
Radiation damage to grape fruit in relation to ethylene production and phenylalanine ammonia-lyase activity.
Radiat Bot
10:
281-286
Romani RJ
(1984)
Respiration, ethylene, senescence, and homeostasis in an integrated view of postharvest life.
Can J Bot
62:
2950-2955
Schiefelbein JW,
Somerville C
(1990)
Genetic control of root hair development in Arabidopsis thaliana.
Plant Cell
2:
235-243
[Abstract/Free Full Text]
Szymanski DB,
Jilk RA,
Pollock SM,
Marks MD
(1998)
Control of GL2 expression in Arabidopsis leaves and trichomes.
Development
125:
1161-1171
[Abstract]
Young RE
(1965)
Effect of ionizing radiation on respiration and ethylene production of avocado fruit.
Nature
205:
1113-1114
[CrossRef][Medline]
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Abstract
Introduction
