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Plant Physiol. (1998) 116: 797-803
Plastid Ontogeny during Petal Development in
Arabidopsis1
Kevin A. Pyke* and
Anton M. Page
School of Biological Sciences, Royal Holloway, University of
London, Egham, Surrey TW20 OEX, United Kingdom
 |
ABSTRACT |
Imaging of chlorophyll
autofluorescence by confocal microscopy in intact whole petals of
Arabidopsis thaliana has been used to analyze
chloroplast development and redifferentiation during petal development.
Young petals dissected from unopened buds contained green chloroplasts
throughout their structure, but as the upper part of the petal lamina
developed and expanded, plastids lost their chlorophyll and
redifferentiated into leukoplasts, resulting in a white petal blade.
Normal green chloroplasts remained in the stalk of the mature petal. In
epidermal cells the chloroplasts were normal and green, in stark
contrast with leaf epidermal cell plastids. In addition, the majority
of these chloroplasts had dumbbell shapes, typical of dividing
chloroplasts, and we suggest that the rapid expansion of petal
epidermal cells may be a trigger for the initiation of chloroplast
division. In petals of the Arabidopsis plastid division mutant
arc6, the conversion of chloroplasts into leukoplasts
was unaffected in spite of the greatly enlarged size and reduced number
of arc6 chloroplasts in cells in the petal base,
resulting in few enlarged leukoplasts in cells from the white lamina of
arc6 petals.
| |
INTRODUCTION |
Studies of the molecular genetic control of plastid
differentiation in the model plant Arabidopsis have focused primarily on the proplastid-to-chloroplast transition during the development of
leaves (Susek et al., 1993 ; Reiter et al., 1994). However, plastids can
undergo several other differentiation pathways, the nature of which is
dependent on the cell type in which the plastid resides. Whereas
several of these differentiation pathways can arise directly from
proplastids in meristem cells, interconversion and redifferentiation of
different plastid types can also occur (Marano et al., 1993). Since the
Arabidopsis model system offers great potential for unraveling the
genetic basis of developmental processes, we have embarked on a study
analyzing a major plastid redifferentiation event that occurs in
Arabidopsis, namely the conversion of chloroplasts into leukoplasts
during petal development.
A major route for chromoplast and leukoplast formation in plants is by
the redifferentiation of chloroplasts, although other pathways of
chromoplast formation directly from proplastids or amyloplasts have
been reported (Marano et al., 1993). The molecular genetic controls of
these processes are poorly understood, although the chromoplast
differentiation pathway, which occurs primarily in ripening fruits of
Solanaceae and Citrus species, has been the most studied
(Mayfield and Huff, 1986; Lawrence et al., 1997). Plastid
differentiation during petal development has been studied with only a
few species, primarily those with yellow petals: Tropaeolum majus (Falk, 1976; Winkenbach et al., 1976), Ranunculus
sp. (Brett and Sommerard, 1986), and Caltha palustris
(Whatley, 1984). Studies of the yellow corollas of cucumber
(Cucumis sativus L.) flowers (Smith and Butler, 1971) have
given rise to a molecular analysis of chromoplast biogenesis in
cucumber (Smirra et al., 1993; Vainstein et al., 1994; Vishnevetsky et
al., 1996). Both pink corollas of petunia (Petunia hybrida)
containing anthocyanin pigment and white petals of Dianthus
caryophyllus have been reported to contain chloroplasts with low
levels of chlorophyll capable of photosynthesis (Weiss et al., 1990;
Weiss and Halevy, 1991; Vainstein and Sharon, 1993).
Although the petals of Arabidopsis thaliana and cresses in
general are white, several other Brassica species have
yellow petals, and in the wallflower (Cheiranthus spp.) a
wide range of red and yellow petal colors exist. The plastids in the
lamina of white petals are colorless, and in this study we have named
them leukoplasts after the terminology of Kirk and Tilney-Bassett
(1978). We also wished to investigate whether mutations that
dramatically affect plastid division and expansion in Arabidopsis leaf
cells interfere with plastid redifferentiation. Foremost among these is
the arc6 mutant (Pyke et al., 1994; Robertson et al., 1995),
in which the leaf mesophyll cells contain only two greatly enlarged
chloroplasts and in which proplastid division in meristematic cells is
also perturbed. Mesophyll chloroplasts are approximately 20-fold
greater in size than the wild type, with highly variable morphology,
and we wanted to determine whether this drastic change in chloroplast number and morphology has any significant affect on the plastid redifferentiation pathway in arc6 petals.
| |
MATERIALS AND METHODS |
Seeds of wild-type Arabidopsis thaliana cv Landsberg
erecta and the arc6 mutant (Pyke et al., 1994;
Robertson et al., 1995) were sown as previously described (Pyke et al.,
1991) and grown under greenhouse conditions, with a daytime temperature
of 20°C, and supplementary lighting to give a photoperiod of 16 h of light and 8 h of darkness. When the plants flowered, buds of
different developmental stages were removed from the main inflorescence and the petals were dissected from the flower bud under a binocular microscope. Plants of the arc6-1 mutant grow normally and
have normal flower and petal morphology, so petals from arc6
plants were harvested in the same manner.
Ultrastructural Analysis of Petals
For analysis of petal structure and plastid ultrastructure within
petal cells, petals were fixed in 3% glutaraldehyde and 4%
formaldehyde in 0.1 m Pipes buffer
(N,N -bis[2-ethanesulfonic acid], pH 7.2),
postfixed in 1% buffered osmium tetroxide, and dehydrated in an
ethanol series prior to embedding in Spurr's resin. To minimize damage
to young petals at early stages of development prior to bud opening,
the entire bud was fixed and sectioned. For analysis of petal-tissue
structure, transverse 0.5-µm-thick sections were cut along the length
of the petal on an ultramicrotome (Cambridge Huxley II), stained with
1% toluidine blue for 5 s at 60°C, and observed using an
Optiphot microscope (Nikon). For the ultrastructural analysis of
plastids, silver sections were cut and stained with uranyl acetate and
Reynold's lead stain and examined using a transmission electron
microscope (model EM109, Zeiss). Anatomical measurements of the petal
structure were carried out directly from mounted sections using a Lucia
image analysis system (Nikon) linked to the Optiphot microscope. A
measurement of cell shape was made using the ratio of the maximum Feret
diameter of the cell transect to the minimum Feret diameter of the cell transect. Feret's diameters of a convex object are the projected lengths of an object at angle  . Lucia measures Feret diameters at
10o intervals through 180o,
and maximum and minimum Feret diameters are the largest and smallest of
these diameter values, respectively. Thus, cell transects tending
toward circularity will have similar values for maximum and minimum
Feret diameters and will have a cell shape value of approximately 1. For long, thin cell transects, the maximum Feret diameter will
approximate cell length and the minimum Feret diameter will approximate
cell width.
Confocal Microscopy
Whole, intact petals were dissected from buds at different
developmental stages, mounted in Vectashield (Vector Laboratories, Peterborough, UK), and examined using a confocal laser-scanning microscope (model TCS 4D, Leica). Red chlorophyll autofluorescence was
visualized in chloroplasts using the tetramethylrhodamine B
isothiocyanate excitation channel. Confocal images were exported to a
PowerPC and montaged using Adobe Photoshop software.
| |
RESULTS |
Anatomy of Petal Development
The four petals of the Arabidopsis flower are initiated at stage 5 of bud development (Smyth et al., 1990), and by stage 9 they have
formed small, flat lamina, which reach to about one-third of stamen
height. Stage 9 was the earliest stage in petal development used in
this study. The structure of the fully expanded petals was relatively
simple, consisting of two single-celled epidermal layers and some
internal mesophyll-like parenchyma cells (Fig. 1). Image analysis of the internal
anatomical structure of mature petals, determined from entire
longitudinal sections of five individual petals, gave a volume
proportion for the epidermis, mesophyll, vascular tissue, and airspace
of 42:30:1:27%, respectively. A simple vascular array was apparent in
fully expanded petals (Fig. 1c), with traces of chlorophyll
fluorescence associated with the vascular strands in the white,
flattened petal lamina. In the flattened upper part of the petal, the
epidermal cells, particularly those on the upper petal surface, were
highly specialized and had a distinct, columnar shape perpendicular to
the axis of the petal (Fig. 1a). In contrast, the epidermal cells
toward the base of the petal were thin and elongated (Fig. 1b).
Analysis of epidermal cell shape in relation to position in the mature
petal (Fig. 2) showed that these two
types of epidermal cells each occupied about 50% of the petal length
and that the point of transition of epidermal cell shape is quite
marked. The elongate morphology of the basal epidermal cells relates to
their rapid expansion, which pushes the petal out of the bud as it
opens. The upper specialized epidermal cells did not expand
significantly during the latter stages of petal development (stage 10 to bud opening), whereas the basal epidermal cells increased on average
approximately 3-fold in length (Fig.
3). From our observations and
measurements of petal anatomy between stage 9 and full expansion, there
was no evidence for cell division within petals during this time, and
the increase in petal size during this period appears to be solely a
result of cell expansion, primarily of the basal epidermal and
mesophyll cells.
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| Figure 1.
Structure of mature Arabidopsis petals. a,
Transverse section through the upper white petal lamina. b, Transverse
section through the stalk at the basal part of the petal. c, Entire
intact petal viewed by conventional fluorescence microscopy showing
chlorophyll autofluorescence in the petal stalk and the lack of
fluorescence in the upper white petal lamina. The extent of the white
petal lamina is shown by the dotted line.
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| Figure 2.
The relationship between the shape of petal
epidermal cells viewed in transverse section and the relative position
of the epidermal cell along the length of mature Arabidopsis petals. Data were collected from three different petals and pooled, since variability between individual petals was very low. Values of cell
shape were maximum. Feret diameter/minimum Feret diameter, see
``Materials and Methods''.
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| Figure 3.
The relationship between the length of epidermal
cells viewed in transverse section and their distance from the petal
base for petals at different developmental stages:  , stage 10;  , stage 12; and  , mature.
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Plastid Development during Petal Expansion
By using chlorophyll autofluorescence and confocal laser-scanning
microscopy on intact petals, we have developed a simple method to
observe individual chloroplasts within petal cells during development.
Young petals at stage 9 dissected from buds contained green
chloroplasts throughout the petal (Fig.
4a). As the petal elongated and expanded,
plastids in the upper portion of the petal, which becomes the flattened
petal lamina, lost their chlorophyll and underwent redifferentiation to
become colorless plastids and were no longer visible in confocal images
(Fig. 4, b-d). Green autofluorescent chloroplasts were maintained in
the lower part of the petal stalk into maturity (Fig. 4d). This green
stalk was maintained largely within the bud, and only the white,
flattened petal lamina was normally observed in intact flowers.
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| Figure 4.
Developing Arabidopsis petals of the wild type
(a-d) and the arc6 mutant (e-h) viewed by confocal
microscopy. Red chlorophyll autofluorescence is shown as gray. The
outline of the white lamina lacking fluorescing plastids is outlined by
dotted lines. a and e, Stage 9; b and f, stage 10; c and g, stage 12;
and d and h, mature.
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In the arc6 mutant, petal development and the spatial
pattern of plastid development were similar to the wild type (Fig. 4), although it can be seen that even at this low magnification individual chloroplasts in the mature petal stalk were larger in arc6
petals than in wild-type petals (Fig. 4, e-h). The density of
chloroplasts in cells from the petal stalk was much lower than that in
leaf mesophyll cells, such that at higher magnification confocal images showed populations of discrete fluorescent chloroplasts (Fig. 5). Since the petal cell walls were not
autofluorescent, it was difficult to count precisely the number of
plastids per cell, but we estimated that the petal cells each contained
15 to 20 fluorescent plastids. Confocal optical sectioning allowed the chloroplasts in the epidermal and mesophyll cell layers to be viewed
separately (Fig. 5, a and b, respectively). Epidermal cell chloroplasts
were slightly smaller than chloroplasts within the internal parenchyma
cells and could be seen in circular arrays (Fig. 5b). These circular
arrays relate to the spatial arrangement of chloroplasts around the
periphery of the conically shaped epidermal cells. In arc6
petals greatly enlarged fluorescent plastids were observed (Fig. 5c),
confirming that this mutant plastid phenotype is maintained during
petal development. Confocal imaging of partly dissected entire buds
revealed that large arc6 plastids were also observed in all
other green floral organs, including the sepals and the style wall
(data not shown).
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| Figure 5.
Confocal images of fluorescing chloroplasts from
the basal part of mature Arabidopsis petals. a, Wild-type mesophyll
parenchyma chloroplasts. b, Wild-type epidermal chloroplasts. c,
arc6 chloroplasts from both epidermal and mesophyll
cells. Arrows in b indicate circular arrays of chloroplasts. Bars = 5 µm.
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To determine how plastids redifferentiate in the white petal blade, the
ultrastructure of plastids in the basal and upper parts of petals was
observed by transmission EM. The redifferentiation of chloroplasts into
leukoplasts in mature wild-type petals is shown in Figure
6. Chloroplasts from cells toward the
petal base had a normal internal thylakoid membrane, similar to
mesophyll chloroplasts, but lacked substantial starch grains (Fig. 6, c and d). In the upper cells from the white petal blade, the leukoplasts were greatly reduced in size and had only remnants of the internal thylakoid membrane system (Fig. 6, a and b). They also contained several osmophilic bodies. This redifferentiation process occurred simultaneously in both mesophyll parenchyma and epidermal cells (Fig.
6). It is especially noteworthy that the epidermal cell chloroplasts in
petals were normal and of a similar size and morphology to leaf
mesophyll chloroplasts, unlike the epidermal cell chloroplasts in
leaves, which are greatly retarded in development and have a much
reduced thylakoid membrane containing low levels of chlorophyll (Dupree
et al., 1991).
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| Figure 6.
Electron micrographs of leukoplasts from the upper
petal lamina (a and b) and chloroplasts from the green stalk of mature wild-type Arabidopsis petals (c and d) in mesophyll parenchyma cells (a
and c) and epidermal cells (b and d). Bars = 1 µm.
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In arc6 petals the redifferentiation of chloroplasts
occurred in a similar way to the wild type (Fig.
7), except that the initial
chloroplasts were greatly enlarged (Fig. 7b) and the resulting leukoplasts were also greatly enlarged compared with the wild-type (Fig. 7a) and yet appeared to have a similar structure, with a residual
amount of thylakoid membrane and some osmophilic bodies. This
development was similar in both arc6 epidermal and mesophyll parenchyma cells. Thus, in spite of the greatly increased plastid size
of arc6 chloroplasts, the redifferentiation of these
plastids into petal leukoplasts was unaffected, resulting in enlarged
leukoplasts. Examination of sectioned arc6 white petal
tissues by transmission EM also showed that these arc6
leukoplasts were rare and difficult to find within cells. Thus, it
appears that a reduced number of leukoplasts exist in cells in the
upper regions of arc6 petals compared with the equivalent
cells in the wild type, in which leukoplasts were more readily
observed.
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| Figure 7.
Electron micrographs of a leukoplast from the
upper white petal lamina (a) and chloroplasts from the green stalk of a
mature Arabidopsis petal (b) of the mutant arc6.
Bars = 1 µm, the same magnification as in Figure 6.
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Plastid Division during Petal Development
During observation of wild-type petal plastids in the basal part
of mature petals, it became obvious that a large proportion of these
chloroplasts showed dumbbell shapes characteristic of dividing
chloroplasts. In high-magnification confocal images, these
dumbbell-shaped plastids were clearly observed (Fig.
8, arrowheads) and made up more than 50%
of the total plastid population. Such dividing plastids were seen in
only these basal cells of the petal stalk, and images of green
chloroplasts at earlier stages of petal development did not show large
numbers of the dumbbell shapes (data not shown). Our observations of
older petals did not show a higher density of distinct chloroplasts in
these cells nor were extended dumbbell-shaped, thin isthmuses observed,
representative of the latter stages of plastid division. Consequently,
it seems unlikely that these chloroplasts complete their division
process to become separate daughter plastids.
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| Figure 8.
Confocal images of fluorescent chloroplasts from
the base of different mature wild-type petals (a and b) showing the
large proportion of the chloroplast population with dumbbell phenotypes typical of chloroplasts in division (arrowheads). Bars = 5 µm.
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| |
DISCUSSION |
We have described, for the first time to our knowledge, the nature
of plastids and their redifferentiation, which occurs during petal
development in Arabidopsis and results in the mature petal having a
white upper lamina that contains colorless leukoplasts and a green
stalk that still contains green chloroplasts. The application of
scanning confocal laser microscopy to analyze plastid development in
petals has proven to be an extremely easy and useful tool. The
relatively low density of green chloroplasts in petal cells compared
with leaf mesophyll cells allows individual chloroplasts to be imaged
with ease. We estimate that in young petal cells there are 15 to 20 chloroplasts per cell, suggesting that little plastid division occurs
in these cells. The redifferentiation into leukoplasts appears to
result in a reduction in plastid number, since at the EM level
leukoplasts are considerably harder to observe in section, although
this may be also partly due to the reduction in size that occurs when
chloroplasts redifferentiate into leukoplasts. A similar reduction in
plastid size also occurs during chloroplast-to-chromoplast redifferentiation in ripening tomato fruit (Pyke, 1997).
A particularly interesting observation is that epidermal cells contain
fully differentiated green chloroplasts with typical internal
morphology. This is in marked contrast to leaf epidermal cells in
Arabidopsis and many other species in which epidermal chloroplasts are
small and poorly developed and contain only low levels of chlorophyll
and other thylakoid-associated proteins (Dupree et al., 1991). All
epidermal cells in the plant arise from the same cell lineage, derived
from the L1 layer in the shoot apical meristem. Petal epidermal cells
are obviously a specialized cell type, in which the repression of
chloroplast development, which occurs in leaf epidermal cells, has been
released. Authentic chloroplast development in petal epidermis is not
confined to the elongate basal epidermal cells but is also observed at
the top of the stalk in mature petals in the specialized conical
epidermal cells, which form primarily on the upper surface of the petal blade. From a functional point of view, presumably, true chloroplasts exist in petal epidermal cells so that the potential for chromoplast differentiation and the production of colored petals is maintained. In
contrast, in the leaf epidermis the presence of mature chloroplasts in
epidermal cells would interfere with light penetration into the leaf
and reduce light-capture efficiency.
We have shown that the arc6 mutation, which results in one
to three greatly enlarged chloroplasts in leaf mesophyll cells, shows a
similar phenotype in young petal cells and the altered chloroplast
morphology and number do not affect the redifferentiation of
arc6 chloroplasts into arc6 leukoplasts. These
observations, coupled with those for arc6 roots (Robertson
et al., 1995), show that alterations in plastid size and morphology, as
manifested by the arc6 mutation, do not affect plastid
differentiation into other types of plastid. This raises the
possibility for the manipulation of other plastid types in plants by
genetic engineering using genes such as arc6 for modifying
the potential for storage in larger plastids or identifying
opportunities for modifying flower color in species with colored
petals.
Although a few anatomical studies have been carried out on plastids
during petal development, mainly in yellow petals, an understanding of
the genetic basis of plastid redifferentiation during petal development
is completely lacking. It should be possible to identify Arabidopsis
mutants in which the pathway of plastid development during petal
development is perturbed, although to our knowledge, no Arabidopsis
mutants with either green or colored petals have been identified to
date. This is surprising considering the extent of mutagenesis and
screening. The production of colored Arabidopsis petals by virtue of
chromoplast formation is likely to require metabolic pathways for the
biosynthesis of pigment molecules, which presumably are lacking in
Arabidopsis. Such pathways must exist in the related domesticated
wallflower (Cheiranthus spp.), since wallflower petal color
is based on variations in red, brown, orange, and yellow. One would
anticipate that true green petals containing chloroplasts, in which the
leukoplast differentiation event has failed to occur, would exist. The
absence of such mutants may suggest that leukoplast differentiation is the default pathway in petal blade cells and that a gain-of-function mutation would be necessary for chloroplasts to be maintained in these
cells.
An interesting feature of chloroplasts in the green petal stalk is the
propensity of dumbbell-shaped profiles. Similar dumbbell-shaped plastids have been observed in other cell types in Arabidopsis (Robertson et al., 1996; Pyke, 1997) and are indicative of an early
stage in plastid division. The biological purpose of dividing plastids
in these cells is unclear, since there is little requirement for a
large population of chloroplasts in this tissue, which has a poor light
environment and initiates senescence within 48 h of full flower
opening, followed rapidly by petal abscission (Smyth et al., 1990).
We have hypothesized that rapid cell expansion and the resulting
reduction in plastid density in cells such as those of the petal stalk
may be a trigger that initiates the plastid division process but does
not necessarily lead to completion (Pyke, 1997). From these studies, it
is apparent that Arabidopsis petals may be a useful and easily
accessible tissue in which to analyze the early stages of the plastid
division process.
| |
FOOTNOTES |
1
This work was supported by the University of
London Central Research Fund.
*
Corresponding author; e-mail k.pyke{at}rhbnc.ac.uk; fax
44-01784-470756.
Received September 2, 1997;
accepted November 13, 1997.
| |
ABBREVIATIONS |
Abbreviation:
EM, electron microscopy.
| |
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Top
Abstract
Introduction