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The molecular and genetic control of ovule development
Kay Schneitz
A genetic approach has resulted in an extensive framework
for the methodical analysis of ovule development. The most
recent progress was accomplished in the areas of
primordium formation and integument morphogenesis.
Furthermore, systematic screens have identified a number of
gametophytic mutations disrupting several distinct steps of
embryo sac ontogenesis.
and the funiculus constitute part of the sporophyte and
hence consist of diploid tissue.
Current Opinion in Plant Biology 1999, 2:13–17
This review focuses on some of the advances achieved in
the past one and a half years. Thus it largely deals with
the control of primordium formation, and the identification and initial genetic characterization of gametophytic
genes which are important for the development of the
embryo sac. By necessity this review is brief; therefore, I
would like to point out a number of recent reviews which
discuss many aspects of ovule development in much
greater detail [3•–6•].
http://biomednet.com/elecref/1369526600200013
The formation of the ovule primordium
© Elsevier Science Ltd ISSN 1369-5266
The initial phase of ovule development encompasses
aspects such as initiation and outgrowth of a protrusion
from the placental tissue, commitment to the ovule fate
and pattern formation in the primordium. The molecular
basis of ovule specification is best understood in Petunia
hybrida where two MADS box genes are known, floral
binding protein 7 (FBP7) and FBP11, that function in this
process, probably in a redundant manner [7,8]. Recently
progress was made in the understanding of the mechanism controlling the outgrowth of the ovule protrusion.
Pattern formation is less well understood; however, some
data begin to shed light on certain aspects of this process
as well.
Addresses
Institute of Plant Biology, University of Zürich, Zollikerstr. 107, CH8008 Zürich, Switzerland; e-mail: [email protected]
Abbreviation
MMC
megaspore mother cell
Introduction
Sexual reproduction constitutes an important event in the
life cycle of a plant. In seed plants the ovule represents
the major female reproductive organ. The ovule carries
the egg cell, it is the organ where fertilization occurs, and
it eventually develops into the seed which harbors the
plant embryo.
For decades, the development of the ovule was only very
poorly understood at the genetic and molecular level.
This situation is changing and the ovules, particularly of
Arabidopsis, but also of Petunia and maize, are now under
thorough investigation. This is partly due to the exciting
biology of the ovule and also due to its suitability to
genetic analysis, which makes the ovule an excellent
model system to study organogenesis in plants.
Mutations in many genes with an important function in
ovule development lead to sterility and this trait is easily scorable in regular mutagenesis experiments. The
current molecular and genetic work is accompanied by
an extensive analysis addressing the evolution of the
basal angiosperm ovule [1,2].
A generalized ovule has a simple but nevertheless highly
differentiated structure (Figures 1 and 2). It develops from
a protrusion of the placental tissue of the gynoecium.
Within the apex or nucellus, the megaspore mother cell
(MMC) develops, undergoes meiosis, and one of the
resulting megaspores gives rise to the multi-cellular haploid embryo sac or female gametophyte which includes the
egg cell. In addition, usually two integuments originate
from a region known as the chalaza. They will grow around
the nucellus and eventually become the seed coat. The
connection to the placenta is made through a stalk or
funiculus. The nucellus, the chalaza with the integuments,
Initiation and outgrowth of the ovule protrusion
In Arabidopsis, the AINTEGUMENTA (ANT) gene acts in
floral organ initiation, growth and shape in general
[9•,10,11,12•]. It encodes a putative transcription factor
[10,11] of the EREBP/AP2 domain class [13]. Compared to
wild type, plants defective for ANT function develop fewer
and more distantly spaced ovules indicating that ANT is
involved in ovule primordium initiation. The ovules that
are produced form a nucellus, chalaza and funiculus, but
lack integuments and an embryo sac.
The typical ant mutant phenotype is caused even by putative null-alleles (the corresponding proteins would be
truncated by about two-thirds) [10,11], suggesting that partially redundant factors regulate ovule primordium
outgrowth. Are such activities known? The HUELLENLOS (HLL) gene [12•] represents one recently described
example [14•] of partially redundant regulation. The phenotype of hll mutants is restricted to the ovule and is
similar to the phenotype of ant mutants as far as the early
block in integument development is concerned. The
analysis of hll ant double mutants revealed the function of
HLL in ovule primordium outgrowth. Plants defective for
HLL and ANT activities bear ovules that are drastically
reduced in their longitudinal or proximal–distal axis.
Either the funiculus or both the funiculus and the chalaza
14
Growth and development
Figure 1
nu
Distal
D
C
Proximal
ch
fu
P
Current Opinion in Plant Biology
fail to form. A nucellus is always present, however. This
implies that HLL and ANT control ovule primordium outgrowth in a partially redundant fashion.
Patterning the primordium
Pattern formation deals with the spatial control of cell fate.
On the basis of morphological criteria, one can recognize a
distinct pattern along a proximal–distal axis of the ovule
[15] (Figure 1). Distally, the nucellus is characterized by the
presence of an MMC, and eventually an embryo sac.
Centrally, the chalaza is recognized as the region that initiates the two integuments at its flank. Proximally, the
funiculus harbors the vascular strand. From an evolutionary
point of view, this is a very conserved pattern and is thus a
typical feature of a generalized seed plant ovule [16].
What mechanism creates the proximal–distal arrangement? We hypothesized that one important aspect is the
setup of a corresponding prepattern, with distal, central
and proximal pattern elements, during the early proliferative phase of primordium formation [15] (for a detailed
discussion see [5•,6•]). Progress on the identification of
genes that directly function in the establishment of the
pattern elements has been scarce. The present data, however, allow one to infer some conclusions about the
patterning process. For example, the BELL1 (BEL1)
expression pattern provides molecular evidence for the
existence of the central pattern element [17]. In addition,
the region-specific defects of many early-acting ovule
genes, for example BEL1, ANT, or INNER NO OUTER
(INO), argue in favor of the presence of such a pattern
[12•]. Furthermore, in hll ant double mutants a nucellus is
present even in the absence of a chalaza and/or funiculus,
which indicates that the distal pattern is independently
formed. This finding also raises the possibility that pattern
formation takes place progressively, beginning at the distal
end of the primordium [14•]. It does not imply, however,
that the formation of the distal element is a prerequisite for
establishing the central and proximal pattern elements.
A scheme outlining wild-type ovule
development in Arabidopsis thaliana and
depicting the postulated proximal–distal
pattern elements. The dashed line indicates a
possible subdivision of the central pattern
element [5•,6•]. The central cartoon omits the
beginning curvature of the ovule at this stage.
The cartoon to the right shows an embryo sac
at a stage after fertilization, but where
fertilization has not taken place. It
corresponds to Figure 2a. The tetrad within
the nucellus, the embryo sac, the integuments
and the vascular strand within the funiculus
are indicated. Abbreviations: C, central
pattern element, ch, chalaza; D, distal pattern
element; fu, funiculus; nu, nucellus; P, proximal
pattern element.
The control of integument development
A number of genes have been identified that are important
for the growth and morphogenesis of the integuments
[4•–6•]. The results indicate that at least two levels of control exist; some genes, such as HLL, ANT or INNER NO
OUTER (INO) are required for the initiation of integuments,
others, including for example SHORT INTEGUMENT1
(SIN1), SUPERMAN (SUP), STRUBBELIG (SUB) and
TSO1, for their morphogenesis. The functions of members
of the first group are likely to precede the activities of members of the second class and in some instances this is
corroborated by genetic analysis [9•]. For example, in corresponding double mutant studies it was shown that ant is
epistatic to sin1, sup and tso1 and ino is epistatic to sup.
The analysis of the later aspects of integument morphogenesis is still in its infancy; however, the results already
foreshadow a complex scenario of multiple distinct steps.
The genes being implicated in these events appear to be
important for cell proliferation and/or cell shape [4•–6•],
and the corresponding mutations lead to an altered morphology of the integuments, rather than to their absence.
As might be expected for genes with a general function in
morphogenesis, members of this class usually exhibit
pleiotropic activities. One example is TOUSLED (TSL)
[18]. Among other functions, TSL appears to control leaf
development, and it promotes specific cell divisions within
the floral meristem as well as the growth of the ovule
integuments [18,19]. TSL is likely to be part of a signal
transduction mechanism as this gene encodes a serine/threonine kinase [19,20•]. A second example is TSO1, which is
also required for flower and ovule development, and which
appears to have a role in cell division and/or directed cell
expansion during floral organogenesis [21,22].
From megaspore mother cell to mature
embryo sac
Gametogenesis can be subdivided into two phases [3•,5•].
Sporogenesis encompasses processes such as megaspore
The molecular and genetic control of ovule development Schneitz
15
Figure 2
Mid-optical sections through mature, wholemount ovules from (a) a male-sterile, (b) an
emd-class mutant and (c) hdd. (a) A postfertilization ovule in the absence of
fertilization. Under normal circumstances
endosperm and embryo development would
already be well underway. The salient
features are indicated. Within the central
cell, the two polar nuclei have fused to yield
a large, di-haploid nucleus. By this stage the
antipodal cells are already degenerated. (b)
The 211E6 mutant [12•]. This sporophytic
mutant exhibits a block at the four-nuclear
embryo sac stage (stage 3-IV [15] or FG4
[39•]). No cellularization occurred. The
sporophytic tissue is apparently normal. (c)
The ovules developed within the same
gynoecium of a plant heterozygous for the
hdd mutation. In the wild-type ovule to the
left, fertilization occurred and an eightnuclear endosperm is present (arrow). In the
hdd-mutant ovule to the right, development
did not proceed beyond the four-nuclear
embryo sac stage (arrow head).
Abbreviations: ap, antipodal cells; cc, central
cell; ec, egg cell; fu, funiculus; ii, inner
integument; oi, outer integument; syn,
synergid; vs, vascular strand. Scale bars,
20 µm
mother cell differentiation and meiosis and eventually
results in a tetrad of megaspores. In most species, only the
proximal or chalazal-most spore will continue development. Megagametogenesis proceeds from this single spore
(monospory) through a syncytial phase, encompassing
three mitoses and elaborate nuclear positioning, followed
by cellularization, to produce a seven-celled Polygonumtype embryo sac [23] (Figure 2).
class of sterile sporophytic mutants, the embryo sac-defective
(emd) mutants [12•], with the corresponding defects apparently restricted to gametophyte development prior to
fertilization (Figure 2). It may be that some of the EMD-class
genes control the establishment of cues in the megaspore
mother cell which are required later during embryo sac
development. Thirdly, the haploid or gametophytic genome
regulates megagametophyte development [29–31].
Sporogenesis
Female gametophytic mutants
In many species, an early step in sporogenesis is the singling out of the prospective MMC from a group of cells in
the nucellar L2 (the first subepidermal) layer. How is this
event regulated? In maize, the mac1 gene is central to this
process [24] — it appears to suppress the commitment to
the gametogenesis pathway in L2 cells other than the
prospective MMC [24].
Until recently, very few female gametophytic mutations
had been described [3•,5•]. In the last few years however,
several laboratories have been successful in isolating and
characterizing a number of gametophytic mutations causing aberrant embryo sac ontogenesis ([3•,5•,32•–34•];
M Hülskamp, personal communication).
The genetic control of the events following MMC commitment is being elucidated as well. Processes, such as
establishment of MMC polarity, meiosis and cytokinesis,
are affected in a number of mutants including switch1
(swi1) in Arabidopsis [25] (C Horlow, personal communication) and ameiotic 1 (am1) in corn [26,27]. Recently, a large
group of genes with a function apparently restricted to
sporogenesis was identified [12 •]. Mutations in this
MEGASPOROGENESIS-DEFECTIVE (MSD) class of
genes lead to a block in gametogenesis at or before the
mono-nuclear embryo sac stage.
Megagametogenesis
The emerging picture of the genetic and molecular control of
female gametophyte ontogenesis is already quite complex.
Firstly, embryo sac development appears to be influenced by
signals coming from the integuments, as many mutants with
a primary defect in integument development also show
altered female gametophyte development [10,11,12•,17,28].
Secondly, it is also possible that the sporophytic genome controls embryo sac formation through a mechanism not
involving the integuments. In Arabidopsis, there exists a large
The successful screens took advantage of two properties of
gametophytic mutations. Usually, female gametophytic
mutations result in an aberrant or unfunctional embryo sac.
As a consequence, 50% of the ovules of a plant heterozygous for a female gametophytic mutation will not develop
into seeds upon fertilization, and thus the plant exhibits
semisterility. Furthermore, the segregation pattern of markers closely linked to the gametophytic mutation deviate
from a typical Mendelian 3:1 ratio. The segregation pattern
can be analyzed in insertion mutants generated by either TDNA or transposons, carrying for example a resistance
marker, or, in experiments involving multiply-marked chromosomes. Additional methods for isolating genes expressed
in the gametophyte include enhancer-trap screens
[5•,35,36] or screens of cDNA libraries prepared from isolated cells of the embryo sac [37,38].
Genes with a function during embryo sac development
include members of the GAMETOPHYTIC FACTOR
(GFA) and FEMALE GAMETOPHYTE (FEM) group of
genes [3•,32•], Gf [39•,40], PROLIFERA (PRL) [35],
ANDARTA (ADA), TISTRYA (TYA) and HADAD (HDD)
(Figure 2) in Arabidopsis [33•,34•] as well as lethal ovule2
16
Growth and development
(lo2) and indeterminate gametophyte1 (ig1) in maize
[41,42,43•]. Some of these genes also have a function during male gametophyte development (for example FEM3
or HDD) and could only be identified because the corresponding mutations are incompletely penetrant.
allowing me to cite unpublished work, Röbi Dudler for comments on the
manuscript and Jay Moore and Ueli Grossniklaus for the hadad mutant
picture. I apologize to the colleagues whose work I could not cite directly
due to space constrictions. Work in my laboratory is supported by the Swiss
National Science Foundation (NF 31-42175.94 and NF 31-53032.97) and by
the Kanton of Zürich.
References and recommended reading
The different mutations lead to blocks at various steps during female gametophyte development. For example, embryo
sacs in the fem2 or ada mutants fail to develop beyond the
mono-nuclear embryo sac stage. Genes like HDD, PRL or lo2
appear primarily to control nuclear division, as the corresponding mutants show embryo sacs variably arrested at the
two-, four or eight-nuclear stage. In the case of PRL this
interpretation is corroborated by sequence information,
because PRL shows homology to genes from yeast encoding
DNA replication initiation factors [35]. Very late aspects of
female gametophyte development are affected in several
mutants [3•]. For example, in gfa2 mutants the two polar
nuclei within the central cell fail to fuse and remain located
side by side. In fem4 mutants, cellularization appears to be
defective, as indicated by the abnormal shapes of the egg
cells and synergids, as well as alterations in number, size and
shape of the vacuoles of these cells.
Conclusions
Recent years have witnessed a remarkable interest in the
molecular and genetic analysis of ovule development.
Much of the present challenge lies in the elucidation of
the molecular structure of the identified sporophytic and
gametophytic genes and the analysis of their genetic
interactions. Besides these immediate concerns a number
of general issues stand out. What genes specify the identity of the Arabidopsis ovule? Although a number of
MADS box genes are candidates [44–46], and APETALA2
(AP2) appears to be involved [47], this significant aspect
is not understood. It will also be important to identify the
genes that regulate patterning in the early ovule primordium and to understand how primordium outgrowth
and pattern formation are orchestrated. Integument morphogenesis is in part characterized by complicated
patterns of cell divisions and cell shape changes. As indicated by the analysis of TSL, signaling pathways are
important in this process. Do genes such as STRUBBELIG (SUB) [12•], SHORT INTEGUMENTS (SIN1)
[48,49], TSO1 and others also encode components of a
signaling mechanism? What connects the signaling
machinery to the cytoskeleton and cell wall, which probably play a crucial role in the regulation of cell shape?
With respect to gametogenesis, the study of the mechanism underlying megasporogenesis will certainly gain
more attention. The analysis of gametophytic mutants
may be complemented by the study of the interplay
between sporophytic and gametophytic factors, which is
likely to occur during female gametophyte development.
Acknowledgements
I thank the members of my lab for stimulating discussions and comments on
the manuscript. I also thank Martin Hülskamp and Christine Horlow for
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
1.
Endress PK: Evolutionary biology of flowers: prospects for the
next century. In Evolution and Diversification of Land Plants. Edited
by Iwatsuki K, Raven PH. Tokyo: Springer; 1997:99-119.
2.
Igersheim A, Endress PK: Gynoecium diversity and systematics of
the paleoherbs. Bot J Linn Soc 1998, 127:289-370.
3. Drews GN, Lee D, Christensen CA: Genetic analysis of female
•
gametophyte development and function. Plant Cell 1998, 10:5-17.
A very clear and detailed summary about the recent conceptual and experimental progress in the genetic analysis of embryo sac development. It
includes a survey of known gametophytic mutants.
Gasser CS, Broadhvest J, Hauser BA: Genetic analysis of ovule
development. Annu Rev Plant Physiol Plant Mol Biol 1998,
49:1-24.
A detailed review focusing on the development of the sporophytic component of the ovule. It features an elaborate genetic model for ovule development (also compare with [6•]) and addresses the evolutionary aspects of
the ovule.
4.
•
Grossniklaus U, Schneitz K: The molecular and genetic basis of
ovule and megagametophyte development. Semin Cell Dev Biol
1998, 9:227-238.
A comprehensive review dealing with the sporophytic as well as the gametophytic aspects of ovule development.
5.
•
Schneitz K, Balasumbramanian S, Schiefthaler U: Organogenesis in
plants: the molecular and genetic control of ovule development.
Trends Plant Sci 1998, 3:468-472.
This review mostly addresses early ovule development in a detailed manner.
It features a genetic model of ovule development (compare with [4•]).
6.
•
7.
Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL,
Dons HJM, van Tunen AJ: A novel class of MADS box genes is
involved in ovule development in Petunia. Plant Cell 1995,
7:1569-1582.
8.
Colombo L, Franken J, Koetje E, van Went J, Dons HJM,
Angenent GC, van Tunen AJ: The Petunia MADS box gene FBP11
determines ovule identity. Plant Cell 1995, 7:1859-1868.
9.
•
Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, Gasser CS:
Interactions among genes regulating ovule development in
Arabidopsis thaliana. Genetics 1997, 145:1109-1124.
An important paper outlining an initial genetic framework of ovule development on the basis of double-mutant analysis. It further provides evidence that
embryo sac development depends on the presence of an inner integument.
10. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes
D, Perez P, Smyth DR: AINTEGUMENTA, an APETALA2-like gene of
Arabidopsis with pleiotropic roles in ovule development and floral
organ growth. Plant Cell 1996, 8:155-168.
11. Klucher KM, Chow H, Reiser L, Fischer RL: The AINTEGUMENTA
gene of Arabidopsis required for ovule and female gametophyte
development is related to the floral homeotic gene APETALA2.
Plant Cell 1996, 8:137-153.
12. Schneitz K, Hülskamp M, Kopczak SD, Pruitt RE: Dissection of
•
sexual organ ontogenesis: a genetic analysis of ovule development
in Arabidopsis thaliana. Development 1997, 124:1367-1376.
A description of a systematic genetic approach to ovule development. The
authors present a survey of a large number of ovule mutants, and, on the
basis of this analysis, introduce a genetic model of ovule development. They
also present indirect evidence for the presence of proximal–distal pattern
formation in the ovule primordium.
13. Okamuro JK, Caster B, Villarroel R, van Montagu M, Jofuku KD: The AP2
domain of APETALA2 defines a large new family of DNA binding
proteins in Arabidopsis. Proc Natl Acad Sci USA 1997, 94:7076-7081.
14. Schneitz K, Baker SC, Gasser CS, Redweik A: Pattern formation
•
and growth during floral organogenesis: HUELLENLOS and
AINTEGUMENTA are required for the formation of the proximal
The molecular and genetic control of ovule development Schneitz
region of the ovule primordium in Arabidopsis thaliana.
Development 1998, 125:2555-2563.
An important paper which directly addresses the genetic control of ovule
primordium outgrowth. It shows that at least two genes, HLL and ANT, regulate the outgrowth of the ovule primordium in a partially redundant manner.
The data provide further evidence for proximal–distal pattern formation in
the ovule primordium and indicate that the distal pattern element forms in
an independent fashion. They also raise the possibility that proximal–distal
patterning takes place progressively and in a distal–proximal direction.
15. Schneitz K, Hülskamp M, Pruitt RE: Wild-type ovule development in
Arabidopsis thaliana: a light microscope study of cleared wholemount tissue. Plant J 1995, 7:731-749.
16. Esau K: Anatomy of Seed Plants. New York: John Wiley & Sons; 1997.
17.
Reiser L, Modrusan Z, L. M, Samach A, Ohad N, Haughn GW, Fischer
RL: The BELL1 gene encodes a homeodomain protein involved in
pattern formation in the Arabidopsis ovule primordium. Cell 1995,
83:735-742.
18. Roe JL, Nemhauser JL, Zambryski PC: TOUSLED participates in
apical tissue formation during gynoecium development in
Arabidopsis. Plant Cell 1997, 9:335-353.
19. Roe JL, Sessions RA, Feldmann KA, Zambryski PC: The Tousled
gene in A. thaliana encodes a protein kinase homolog that is
required for leaf and flower development. Cell 1993, 75:939-950.
20. Roe JL, Durfee T, Zupan JR, Repetti P, McLean BG, Zambryski PC:
•
TOUSLED is a nuclear serine/threonine protein kinase that
requires a coiled-coil region for oligomerization and catalytic
activity. J Biol Chem 1997, 272:5838-5845.
The authors provide evidence that TSL encodes a nuclear serine-threonine
kinase. Activation of the protein kinase seems to require interaction between
TSL molecules.
21. Liu Z, Running M, Meyerowitz EM: TSO1 functions in cell division
during Arabidopsis flower development. Development 1997,
124:665-672.
22. Hauser BA, Villanueva JM, Gasser CS: Arabidopsis TSO1 regulates
directional processes in cells during floral organogenesis.
Genetics 1998, 150:411-423.
23. Maheswari P: An Introduction to the Embryology of Angiosperms.
New York: McGraw-Hill; 1950.
24. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya
IN: The mac1 gene: controlling the commitment to the meiotic
pathway in maize. Genetics 1996, 142:1009-1020.
25. Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O,
Marchand M, Bechtold N, Pelletier G, Horlow C: switch (swi1), an
Arabidopsis thaliana mutant effected in the female meiotic
switch. Abstract 307, 9th International Conference on Arabidopsis
Research, 24-28 June 1998. Madison WI.
26. Golubovskaya IN, Avaklinka N, Sheridan W: Effects of several meiotic
mutants on female meiosis in maize. Dev Genet 1992, 13:411-424.
27.
Golubovskaya I, Avalkina N, Sheridan WF: New insights into the role
of the maize ameiotic1 locus. Genetics 1997, 147:1339-1350.
28. Reiser L, Fischer RL: The ovule and the embryo sac. Plant Cell
1993, 5:1291-1301.
29. Patterson EB: Translocations as genetic markers. In The Maize
Handbook. New York: Springer; 1994:361-363.
30. Vizir IY, Anderson ML, Wilson ZA, Mulligan BJ: Isolation of
deficiencies in the Arabidopsis genome by g-irradiation of pollen.
Genetics 1994, 137:1111-1119.
31. Vollbrecht E, Hake S: Deficiency analysis of female gametogenesis
in maize. Dev Genet 1995, 16:44-63.
32. Feldmann KA, Coury DA, Christianson ML: Exceptional segregation
•
of a selectable marker (KanR) in Arabidopsis identifies genes
important for gametophytic growth and development. Genetics
1997, 147:1411-1422.
The first report of a systematic analysis of segregation ratio distortions in a
population of T-DNA-induced mutant lines in Arabidopsis. This work led to
the identification of seven gametophytic genes.
17
33. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D:
•
Selection of T-DNA-tagged male and female gametophytic
mutants by segregation distortion in Arabidopsis. Genetics 1998,
149:621-631.
A similar study as in [32•]. It includes a phenotypic description of two female
gametophytic mutants. In both cases the viable megaspore does not initiate
the nuclear division cycles.
34. Moore JM, Vielle Calzada J-P, Gagliano W, Grossniklaus U: Genetic
•
characterization of hadad, a mutant disrupting female
gametogenesis in Arabidopsis thaliana. Cold Spring Harbor Symp
Quant Biol 1997, 62:35-47.
The authors describe the isolation of the gametophytic hadad mutation by a
transposon-induced (gene-trap) mutagenesis screen. The hdd mutants
exhibit an aberrant segregation ratio and reduced seed set. The embryo sac
is predominantly affected and the results indicate that HDD is required for
the correct progression through the mitotic division cycles.
35. Springer PS, McCombie R, Sundaresan V, Martienssen RA: Gene
trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in
Arabidopsis. Science 1995, 268:877-880.
36. Sundaresan V, Springer P, Volpe T, Haward S, Jones J, Dean C, Ma H,
Martiensen R: Patterns of gene action in plant development
revealed by enhancer trap and gene trap transposable elements.
Genes Dev 1995, 9:1797-1810.
37.
Dresselhaus T, Lörz H, Kranz E: Representative cDNA libraries from
few plant cells. Plant J 1994, 5:605-610.
38. Kranz E, Dresselhaus T: In vitro fertilization with isolated higher
plant gametes. Trends Plant Sci 1996, 1:82-89.
39. Christensen CA, King EJ, Jordan JR, Drews GN:
•
Megagametogenesis in Arabidopsis wild type and the Gf mutant.
Sex Plant Reprod 1997, 10:49-64.
An excellent description of embryo sac development in Arabidopsis using
confocal laser scanning microscopy. Analysis of the Gf mutant indicates
a very early role for the corresponding gene in wild-type embryo
sac ontogenesis.
40. Rédei GP: Non-mendelian megagametogenesis in Arabidopsis.
Genetics 1965, 51:857-872.
41. Huang B-Q, Sheridan WF: Embryo sac development in the maize
indeterminate gametophyte1 mutant: abnormal nuclear behavior
and defective microtubule organization. Plant Cell 1996,
8:1391-1407.
42. Kermicle JL: Pleiotropic effects on seed development of the
indeterminate gametophyte gene in maize. Amer J Bot 1971, 58:1-7.
43. Sheridan WF, Huang B-Q: Nuclear behavior is defective in the
•
maize (Zea mays L.) lethal ovule2 female gametophyte. Plant J
1997, 11:1029-1041.
A careful analysis of the mutant phenotype using fluorescent microscopy.
The results indicate that lethal ovule2 is essential for nuclear division, migration and the accompanying tubulin cytoskeleton behavior during maize
embryo sac development.
44. Ma H, Yanofsky MF, Meyerowitz EM: AGL1-ALG6, an Arabidopsis
gene family with similarity to floral homeotic and transcription
factor genes. Genes Dev 1991, 5:484-495.
45. Rounsley SD, Ditta GS, Yanofsky MF: Diverse roles for MADS
box genes in Arabidopsis development. Plant Cell 1995,
7:1259-1269.
46. Savidge B, Rounsley SD, Yanofsky M: Temporal relationship
between the transcription of two Arabidopsis MADS box genes
and the floral organ identity genes. Plant Cell 1995, 7:721-733.
47.
Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW:
Homeotic transformation of ovules into carpel-like structures in
Arabidopsis. Plant Cell 1994, 6:333-349.
48. Robinson-Beers K, Pruitt RE, Gasser CS: Ovule development in
wild-type Arabidopsis and two female-sterile mutants. Plant Cell
1992, 4:1237-1249.
49. Lang JD, Ray S, Ray A: sin1, a mutation affecting female fertility in
Arabidopsis, interacts with mod1, its recessive modifier. Genetics
1994, 137:1101-1110.
The molecular and genetic control of ovule development
Kay Schneitz
A genetic approach has resulted in an extensive framework
for the methodical analysis of ovule development. The most
recent progress was accomplished in the areas of
primordium formation and integument morphogenesis.
Furthermore, systematic screens have identified a number of
gametophytic mutations disrupting several distinct steps of
embryo sac ontogenesis.
and the funiculus constitute part of the sporophyte and
hence consist of diploid tissue.
Current Opinion in Plant Biology 1999, 2:13–17
This review focuses on some of the advances achieved in
the past one and a half years. Thus it largely deals with
the control of primordium formation, and the identification and initial genetic characterization of gametophytic
genes which are important for the development of the
embryo sac. By necessity this review is brief; therefore, I
would like to point out a number of recent reviews which
discuss many aspects of ovule development in much
greater detail [3•–6•].
http://biomednet.com/elecref/1369526600200013
The formation of the ovule primordium
© Elsevier Science Ltd ISSN 1369-5266
The initial phase of ovule development encompasses
aspects such as initiation and outgrowth of a protrusion
from the placental tissue, commitment to the ovule fate
and pattern formation in the primordium. The molecular
basis of ovule specification is best understood in Petunia
hybrida where two MADS box genes are known, floral
binding protein 7 (FBP7) and FBP11, that function in this
process, probably in a redundant manner [7,8]. Recently
progress was made in the understanding of the mechanism controlling the outgrowth of the ovule protrusion.
Pattern formation is less well understood; however, some
data begin to shed light on certain aspects of this process
as well.
Addresses
Institute of Plant Biology, University of Zürich, Zollikerstr. 107, CH8008 Zürich, Switzerland; e-mail: [email protected]
Abbreviation
MMC
megaspore mother cell
Introduction
Sexual reproduction constitutes an important event in the
life cycle of a plant. In seed plants the ovule represents
the major female reproductive organ. The ovule carries
the egg cell, it is the organ where fertilization occurs, and
it eventually develops into the seed which harbors the
plant embryo.
For decades, the development of the ovule was only very
poorly understood at the genetic and molecular level.
This situation is changing and the ovules, particularly of
Arabidopsis, but also of Petunia and maize, are now under
thorough investigation. This is partly due to the exciting
biology of the ovule and also due to its suitability to
genetic analysis, which makes the ovule an excellent
model system to study organogenesis in plants.
Mutations in many genes with an important function in
ovule development lead to sterility and this trait is easily scorable in regular mutagenesis experiments. The
current molecular and genetic work is accompanied by
an extensive analysis addressing the evolution of the
basal angiosperm ovule [1,2].
A generalized ovule has a simple but nevertheless highly
differentiated structure (Figures 1 and 2). It develops from
a protrusion of the placental tissue of the gynoecium.
Within the apex or nucellus, the megaspore mother cell
(MMC) develops, undergoes meiosis, and one of the
resulting megaspores gives rise to the multi-cellular haploid embryo sac or female gametophyte which includes the
egg cell. In addition, usually two integuments originate
from a region known as the chalaza. They will grow around
the nucellus and eventually become the seed coat. The
connection to the placenta is made through a stalk or
funiculus. The nucellus, the chalaza with the integuments,
Initiation and outgrowth of the ovule protrusion
In Arabidopsis, the AINTEGUMENTA (ANT) gene acts in
floral organ initiation, growth and shape in general
[9•,10,11,12•]. It encodes a putative transcription factor
[10,11] of the EREBP/AP2 domain class [13]. Compared to
wild type, plants defective for ANT function develop fewer
and more distantly spaced ovules indicating that ANT is
involved in ovule primordium initiation. The ovules that
are produced form a nucellus, chalaza and funiculus, but
lack integuments and an embryo sac.
The typical ant mutant phenotype is caused even by putative null-alleles (the corresponding proteins would be
truncated by about two-thirds) [10,11], suggesting that partially redundant factors regulate ovule primordium
outgrowth. Are such activities known? The HUELLENLOS (HLL) gene [12•] represents one recently described
example [14•] of partially redundant regulation. The phenotype of hll mutants is restricted to the ovule and is
similar to the phenotype of ant mutants as far as the early
block in integument development is concerned. The
analysis of hll ant double mutants revealed the function of
HLL in ovule primordium outgrowth. Plants defective for
HLL and ANT activities bear ovules that are drastically
reduced in their longitudinal or proximal–distal axis.
Either the funiculus or both the funiculus and the chalaza
14
Growth and development
Figure 1
nu
Distal
D
C
Proximal
ch
fu
P
Current Opinion in Plant Biology
fail to form. A nucellus is always present, however. This
implies that HLL and ANT control ovule primordium outgrowth in a partially redundant fashion.
Patterning the primordium
Pattern formation deals with the spatial control of cell fate.
On the basis of morphological criteria, one can recognize a
distinct pattern along a proximal–distal axis of the ovule
[15] (Figure 1). Distally, the nucellus is characterized by the
presence of an MMC, and eventually an embryo sac.
Centrally, the chalaza is recognized as the region that initiates the two integuments at its flank. Proximally, the
funiculus harbors the vascular strand. From an evolutionary
point of view, this is a very conserved pattern and is thus a
typical feature of a generalized seed plant ovule [16].
What mechanism creates the proximal–distal arrangement? We hypothesized that one important aspect is the
setup of a corresponding prepattern, with distal, central
and proximal pattern elements, during the early proliferative phase of primordium formation [15] (for a detailed
discussion see [5•,6•]). Progress on the identification of
genes that directly function in the establishment of the
pattern elements has been scarce. The present data, however, allow one to infer some conclusions about the
patterning process. For example, the BELL1 (BEL1)
expression pattern provides molecular evidence for the
existence of the central pattern element [17]. In addition,
the region-specific defects of many early-acting ovule
genes, for example BEL1, ANT, or INNER NO OUTER
(INO), argue in favor of the presence of such a pattern
[12•]. Furthermore, in hll ant double mutants a nucellus is
present even in the absence of a chalaza and/or funiculus,
which indicates that the distal pattern is independently
formed. This finding also raises the possibility that pattern
formation takes place progressively, beginning at the distal
end of the primordium [14•]. It does not imply, however,
that the formation of the distal element is a prerequisite for
establishing the central and proximal pattern elements.
A scheme outlining wild-type ovule
development in Arabidopsis thaliana and
depicting the postulated proximal–distal
pattern elements. The dashed line indicates a
possible subdivision of the central pattern
element [5•,6•]. The central cartoon omits the
beginning curvature of the ovule at this stage.
The cartoon to the right shows an embryo sac
at a stage after fertilization, but where
fertilization has not taken place. It
corresponds to Figure 2a. The tetrad within
the nucellus, the embryo sac, the integuments
and the vascular strand within the funiculus
are indicated. Abbreviations: C, central
pattern element, ch, chalaza; D, distal pattern
element; fu, funiculus; nu, nucellus; P, proximal
pattern element.
The control of integument development
A number of genes have been identified that are important
for the growth and morphogenesis of the integuments
[4•–6•]. The results indicate that at least two levels of control exist; some genes, such as HLL, ANT or INNER NO
OUTER (INO) are required for the initiation of integuments,
others, including for example SHORT INTEGUMENT1
(SIN1), SUPERMAN (SUP), STRUBBELIG (SUB) and
TSO1, for their morphogenesis. The functions of members
of the first group are likely to precede the activities of members of the second class and in some instances this is
corroborated by genetic analysis [9•]. For example, in corresponding double mutant studies it was shown that ant is
epistatic to sin1, sup and tso1 and ino is epistatic to sup.
The analysis of the later aspects of integument morphogenesis is still in its infancy; however, the results already
foreshadow a complex scenario of multiple distinct steps.
The genes being implicated in these events appear to be
important for cell proliferation and/or cell shape [4•–6•],
and the corresponding mutations lead to an altered morphology of the integuments, rather than to their absence.
As might be expected for genes with a general function in
morphogenesis, members of this class usually exhibit
pleiotropic activities. One example is TOUSLED (TSL)
[18]. Among other functions, TSL appears to control leaf
development, and it promotes specific cell divisions within
the floral meristem as well as the growth of the ovule
integuments [18,19]. TSL is likely to be part of a signal
transduction mechanism as this gene encodes a serine/threonine kinase [19,20•]. A second example is TSO1, which is
also required for flower and ovule development, and which
appears to have a role in cell division and/or directed cell
expansion during floral organogenesis [21,22].
From megaspore mother cell to mature
embryo sac
Gametogenesis can be subdivided into two phases [3•,5•].
Sporogenesis encompasses processes such as megaspore
The molecular and genetic control of ovule development Schneitz
15
Figure 2
Mid-optical sections through mature, wholemount ovules from (a) a male-sterile, (b) an
emd-class mutant and (c) hdd. (a) A postfertilization ovule in the absence of
fertilization. Under normal circumstances
endosperm and embryo development would
already be well underway. The salient
features are indicated. Within the central
cell, the two polar nuclei have fused to yield
a large, di-haploid nucleus. By this stage the
antipodal cells are already degenerated. (b)
The 211E6 mutant [12•]. This sporophytic
mutant exhibits a block at the four-nuclear
embryo sac stage (stage 3-IV [15] or FG4
[39•]). No cellularization occurred. The
sporophytic tissue is apparently normal. (c)
The ovules developed within the same
gynoecium of a plant heterozygous for the
hdd mutation. In the wild-type ovule to the
left, fertilization occurred and an eightnuclear endosperm is present (arrow). In the
hdd-mutant ovule to the right, development
did not proceed beyond the four-nuclear
embryo sac stage (arrow head).
Abbreviations: ap, antipodal cells; cc, central
cell; ec, egg cell; fu, funiculus; ii, inner
integument; oi, outer integument; syn,
synergid; vs, vascular strand. Scale bars,
20 µm
mother cell differentiation and meiosis and eventually
results in a tetrad of megaspores. In most species, only the
proximal or chalazal-most spore will continue development. Megagametogenesis proceeds from this single spore
(monospory) through a syncytial phase, encompassing
three mitoses and elaborate nuclear positioning, followed
by cellularization, to produce a seven-celled Polygonumtype embryo sac [23] (Figure 2).
class of sterile sporophytic mutants, the embryo sac-defective
(emd) mutants [12•], with the corresponding defects apparently restricted to gametophyte development prior to
fertilization (Figure 2). It may be that some of the EMD-class
genes control the establishment of cues in the megaspore
mother cell which are required later during embryo sac
development. Thirdly, the haploid or gametophytic genome
regulates megagametophyte development [29–31].
Sporogenesis
Female gametophytic mutants
In many species, an early step in sporogenesis is the singling out of the prospective MMC from a group of cells in
the nucellar L2 (the first subepidermal) layer. How is this
event regulated? In maize, the mac1 gene is central to this
process [24] — it appears to suppress the commitment to
the gametogenesis pathway in L2 cells other than the
prospective MMC [24].
Until recently, very few female gametophytic mutations
had been described [3•,5•]. In the last few years however,
several laboratories have been successful in isolating and
characterizing a number of gametophytic mutations causing aberrant embryo sac ontogenesis ([3•,5•,32•–34•];
M Hülskamp, personal communication).
The genetic control of the events following MMC commitment is being elucidated as well. Processes, such as
establishment of MMC polarity, meiosis and cytokinesis,
are affected in a number of mutants including switch1
(swi1) in Arabidopsis [25] (C Horlow, personal communication) and ameiotic 1 (am1) in corn [26,27]. Recently, a large
group of genes with a function apparently restricted to
sporogenesis was identified [12 •]. Mutations in this
MEGASPOROGENESIS-DEFECTIVE (MSD) class of
genes lead to a block in gametogenesis at or before the
mono-nuclear embryo sac stage.
Megagametogenesis
The emerging picture of the genetic and molecular control of
female gametophyte ontogenesis is already quite complex.
Firstly, embryo sac development appears to be influenced by
signals coming from the integuments, as many mutants with
a primary defect in integument development also show
altered female gametophyte development [10,11,12•,17,28].
Secondly, it is also possible that the sporophytic genome controls embryo sac formation through a mechanism not
involving the integuments. In Arabidopsis, there exists a large
The successful screens took advantage of two properties of
gametophytic mutations. Usually, female gametophytic
mutations result in an aberrant or unfunctional embryo sac.
As a consequence, 50% of the ovules of a plant heterozygous for a female gametophytic mutation will not develop
into seeds upon fertilization, and thus the plant exhibits
semisterility. Furthermore, the segregation pattern of markers closely linked to the gametophytic mutation deviate
from a typical Mendelian 3:1 ratio. The segregation pattern
can be analyzed in insertion mutants generated by either TDNA or transposons, carrying for example a resistance
marker, or, in experiments involving multiply-marked chromosomes. Additional methods for isolating genes expressed
in the gametophyte include enhancer-trap screens
[5•,35,36] or screens of cDNA libraries prepared from isolated cells of the embryo sac [37,38].
Genes with a function during embryo sac development
include members of the GAMETOPHYTIC FACTOR
(GFA) and FEMALE GAMETOPHYTE (FEM) group of
genes [3•,32•], Gf [39•,40], PROLIFERA (PRL) [35],
ANDARTA (ADA), TISTRYA (TYA) and HADAD (HDD)
(Figure 2) in Arabidopsis [33•,34•] as well as lethal ovule2
16
Growth and development
(lo2) and indeterminate gametophyte1 (ig1) in maize
[41,42,43•]. Some of these genes also have a function during male gametophyte development (for example FEM3
or HDD) and could only be identified because the corresponding mutations are incompletely penetrant.
allowing me to cite unpublished work, Röbi Dudler for comments on the
manuscript and Jay Moore and Ueli Grossniklaus for the hadad mutant
picture. I apologize to the colleagues whose work I could not cite directly
due to space constrictions. Work in my laboratory is supported by the Swiss
National Science Foundation (NF 31-42175.94 and NF 31-53032.97) and by
the Kanton of Zürich.
References and recommended reading
The different mutations lead to blocks at various steps during female gametophyte development. For example, embryo
sacs in the fem2 or ada mutants fail to develop beyond the
mono-nuclear embryo sac stage. Genes like HDD, PRL or lo2
appear primarily to control nuclear division, as the corresponding mutants show embryo sacs variably arrested at the
two-, four or eight-nuclear stage. In the case of PRL this
interpretation is corroborated by sequence information,
because PRL shows homology to genes from yeast encoding
DNA replication initiation factors [35]. Very late aspects of
female gametophyte development are affected in several
mutants [3•]. For example, in gfa2 mutants the two polar
nuclei within the central cell fail to fuse and remain located
side by side. In fem4 mutants, cellularization appears to be
defective, as indicated by the abnormal shapes of the egg
cells and synergids, as well as alterations in number, size and
shape of the vacuoles of these cells.
Conclusions
Recent years have witnessed a remarkable interest in the
molecular and genetic analysis of ovule development.
Much of the present challenge lies in the elucidation of
the molecular structure of the identified sporophytic and
gametophytic genes and the analysis of their genetic
interactions. Besides these immediate concerns a number
of general issues stand out. What genes specify the identity of the Arabidopsis ovule? Although a number of
MADS box genes are candidates [44–46], and APETALA2
(AP2) appears to be involved [47], this significant aspect
is not understood. It will also be important to identify the
genes that regulate patterning in the early ovule primordium and to understand how primordium outgrowth
and pattern formation are orchestrated. Integument morphogenesis is in part characterized by complicated
patterns of cell divisions and cell shape changes. As indicated by the analysis of TSL, signaling pathways are
important in this process. Do genes such as STRUBBELIG (SUB) [12•], SHORT INTEGUMENTS (SIN1)
[48,49], TSO1 and others also encode components of a
signaling mechanism? What connects the signaling
machinery to the cytoskeleton and cell wall, which probably play a crucial role in the regulation of cell shape?
With respect to gametogenesis, the study of the mechanism underlying megasporogenesis will certainly gain
more attention. The analysis of gametophytic mutants
may be complemented by the study of the interplay
between sporophytic and gametophytic factors, which is
likely to occur during female gametophyte development.
Acknowledgements
I thank the members of my lab for stimulating discussions and comments on
the manuscript. I also thank Martin Hülskamp and Christine Horlow for
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
1.
Endress PK: Evolutionary biology of flowers: prospects for the
next century. In Evolution and Diversification of Land Plants. Edited
by Iwatsuki K, Raven PH. Tokyo: Springer; 1997:99-119.
2.
Igersheim A, Endress PK: Gynoecium diversity and systematics of
the paleoherbs. Bot J Linn Soc 1998, 127:289-370.
3. Drews GN, Lee D, Christensen CA: Genetic analysis of female
•
gametophyte development and function. Plant Cell 1998, 10:5-17.
A very clear and detailed summary about the recent conceptual and experimental progress in the genetic analysis of embryo sac development. It
includes a survey of known gametophytic mutants.
Gasser CS, Broadhvest J, Hauser BA: Genetic analysis of ovule
development. Annu Rev Plant Physiol Plant Mol Biol 1998,
49:1-24.
A detailed review focusing on the development of the sporophytic component of the ovule. It features an elaborate genetic model for ovule development (also compare with [6•]) and addresses the evolutionary aspects of
the ovule.
4.
•
Grossniklaus U, Schneitz K: The molecular and genetic basis of
ovule and megagametophyte development. Semin Cell Dev Biol
1998, 9:227-238.
A comprehensive review dealing with the sporophytic as well as the gametophytic aspects of ovule development.
5.
•
Schneitz K, Balasumbramanian S, Schiefthaler U: Organogenesis in
plants: the molecular and genetic control of ovule development.
Trends Plant Sci 1998, 3:468-472.
This review mostly addresses early ovule development in a detailed manner.
It features a genetic model of ovule development (compare with [4•]).
6.
•
7.
Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL,
Dons HJM, van Tunen AJ: A novel class of MADS box genes is
involved in ovule development in Petunia. Plant Cell 1995,
7:1569-1582.
8.
Colombo L, Franken J, Koetje E, van Went J, Dons HJM,
Angenent GC, van Tunen AJ: The Petunia MADS box gene FBP11
determines ovule identity. Plant Cell 1995, 7:1859-1868.
9.
•
Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, Gasser CS:
Interactions among genes regulating ovule development in
Arabidopsis thaliana. Genetics 1997, 145:1109-1124.
An important paper outlining an initial genetic framework of ovule development on the basis of double-mutant analysis. It further provides evidence that
embryo sac development depends on the presence of an inner integument.
10. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes
D, Perez P, Smyth DR: AINTEGUMENTA, an APETALA2-like gene of
Arabidopsis with pleiotropic roles in ovule development and floral
organ growth. Plant Cell 1996, 8:155-168.
11. Klucher KM, Chow H, Reiser L, Fischer RL: The AINTEGUMENTA
gene of Arabidopsis required for ovule and female gametophyte
development is related to the floral homeotic gene APETALA2.
Plant Cell 1996, 8:137-153.
12. Schneitz K, Hülskamp M, Kopczak SD, Pruitt RE: Dissection of
•
sexual organ ontogenesis: a genetic analysis of ovule development
in Arabidopsis thaliana. Development 1997, 124:1367-1376.
A description of a systematic genetic approach to ovule development. The
authors present a survey of a large number of ovule mutants, and, on the
basis of this analysis, introduce a genetic model of ovule development. They
also present indirect evidence for the presence of proximal–distal pattern
formation in the ovule primordium.
13. Okamuro JK, Caster B, Villarroel R, van Montagu M, Jofuku KD: The AP2
domain of APETALA2 defines a large new family of DNA binding
proteins in Arabidopsis. Proc Natl Acad Sci USA 1997, 94:7076-7081.
14. Schneitz K, Baker SC, Gasser CS, Redweik A: Pattern formation
•
and growth during floral organogenesis: HUELLENLOS and
AINTEGUMENTA are required for the formation of the proximal
The molecular and genetic control of ovule development Schneitz
region of the ovule primordium in Arabidopsis thaliana.
Development 1998, 125:2555-2563.
An important paper which directly addresses the genetic control of ovule
primordium outgrowth. It shows that at least two genes, HLL and ANT, regulate the outgrowth of the ovule primordium in a partially redundant manner.
The data provide further evidence for proximal–distal pattern formation in
the ovule primordium and indicate that the distal pattern element forms in
an independent fashion. They also raise the possibility that proximal–distal
patterning takes place progressively and in a distal–proximal direction.
15. Schneitz K, Hülskamp M, Pruitt RE: Wild-type ovule development in
Arabidopsis thaliana: a light microscope study of cleared wholemount tissue. Plant J 1995, 7:731-749.
16. Esau K: Anatomy of Seed Plants. New York: John Wiley & Sons; 1997.
17.
Reiser L, Modrusan Z, L. M, Samach A, Ohad N, Haughn GW, Fischer
RL: The BELL1 gene encodes a homeodomain protein involved in
pattern formation in the Arabidopsis ovule primordium. Cell 1995,
83:735-742.
18. Roe JL, Nemhauser JL, Zambryski PC: TOUSLED participates in
apical tissue formation during gynoecium development in
Arabidopsis. Plant Cell 1997, 9:335-353.
19. Roe JL, Sessions RA, Feldmann KA, Zambryski PC: The Tousled
gene in A. thaliana encodes a protein kinase homolog that is
required for leaf and flower development. Cell 1993, 75:939-950.
20. Roe JL, Durfee T, Zupan JR, Repetti P, McLean BG, Zambryski PC:
•
TOUSLED is a nuclear serine/threonine protein kinase that
requires a coiled-coil region for oligomerization and catalytic
activity. J Biol Chem 1997, 272:5838-5845.
The authors provide evidence that TSL encodes a nuclear serine-threonine
kinase. Activation of the protein kinase seems to require interaction between
TSL molecules.
21. Liu Z, Running M, Meyerowitz EM: TSO1 functions in cell division
during Arabidopsis flower development. Development 1997,
124:665-672.
22. Hauser BA, Villanueva JM, Gasser CS: Arabidopsis TSO1 regulates
directional processes in cells during floral organogenesis.
Genetics 1998, 150:411-423.
23. Maheswari P: An Introduction to the Embryology of Angiosperms.
New York: McGraw-Hill; 1950.
24. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya
IN: The mac1 gene: controlling the commitment to the meiotic
pathway in maize. Genetics 1996, 142:1009-1020.
25. Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O,
Marchand M, Bechtold N, Pelletier G, Horlow C: switch (swi1), an
Arabidopsis thaliana mutant effected in the female meiotic
switch. Abstract 307, 9th International Conference on Arabidopsis
Research, 24-28 June 1998. Madison WI.
26. Golubovskaya IN, Avaklinka N, Sheridan W: Effects of several meiotic
mutants on female meiosis in maize. Dev Genet 1992, 13:411-424.
27.
Golubovskaya I, Avalkina N, Sheridan WF: New insights into the role
of the maize ameiotic1 locus. Genetics 1997, 147:1339-1350.
28. Reiser L, Fischer RL: The ovule and the embryo sac. Plant Cell
1993, 5:1291-1301.
29. Patterson EB: Translocations as genetic markers. In The Maize
Handbook. New York: Springer; 1994:361-363.
30. Vizir IY, Anderson ML, Wilson ZA, Mulligan BJ: Isolation of
deficiencies in the Arabidopsis genome by g-irradiation of pollen.
Genetics 1994, 137:1111-1119.
31. Vollbrecht E, Hake S: Deficiency analysis of female gametogenesis
in maize. Dev Genet 1995, 16:44-63.
32. Feldmann KA, Coury DA, Christianson ML: Exceptional segregation
•
of a selectable marker (KanR) in Arabidopsis identifies genes
important for gametophytic growth and development. Genetics
1997, 147:1411-1422.
The first report of a systematic analysis of segregation ratio distortions in a
population of T-DNA-induced mutant lines in Arabidopsis. This work led to
the identification of seven gametophytic genes.
17
33. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D:
•
Selection of T-DNA-tagged male and female gametophytic
mutants by segregation distortion in Arabidopsis. Genetics 1998,
149:621-631.
A similar study as in [32•]. It includes a phenotypic description of two female
gametophytic mutants. In both cases the viable megaspore does not initiate
the nuclear division cycles.
34. Moore JM, Vielle Calzada J-P, Gagliano W, Grossniklaus U: Genetic
•
characterization of hadad, a mutant disrupting female
gametogenesis in Arabidopsis thaliana. Cold Spring Harbor Symp
Quant Biol 1997, 62:35-47.
The authors describe the isolation of the gametophytic hadad mutation by a
transposon-induced (gene-trap) mutagenesis screen. The hdd mutants
exhibit an aberrant segregation ratio and reduced seed set. The embryo sac
is predominantly affected and the results indicate that HDD is required for
the correct progression through the mitotic division cycles.
35. Springer PS, McCombie R, Sundaresan V, Martienssen RA: Gene
trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in
Arabidopsis. Science 1995, 268:877-880.
36. Sundaresan V, Springer P, Volpe T, Haward S, Jones J, Dean C, Ma H,
Martiensen R: Patterns of gene action in plant development
revealed by enhancer trap and gene trap transposable elements.
Genes Dev 1995, 9:1797-1810.
37.
Dresselhaus T, Lörz H, Kranz E: Representative cDNA libraries from
few plant cells. Plant J 1994, 5:605-610.
38. Kranz E, Dresselhaus T: In vitro fertilization with isolated higher
plant gametes. Trends Plant Sci 1996, 1:82-89.
39. Christensen CA, King EJ, Jordan JR, Drews GN:
•
Megagametogenesis in Arabidopsis wild type and the Gf mutant.
Sex Plant Reprod 1997, 10:49-64.
An excellent description of embryo sac development in Arabidopsis using
confocal laser scanning microscopy. Analysis of the Gf mutant indicates
a very early role for the corresponding gene in wild-type embryo
sac ontogenesis.
40. Rédei GP: Non-mendelian megagametogenesis in Arabidopsis.
Genetics 1965, 51:857-872.
41. Huang B-Q, Sheridan WF: Embryo sac development in the maize
indeterminate gametophyte1 mutant: abnormal nuclear behavior
and defective microtubule organization. Plant Cell 1996,
8:1391-1407.
42. Kermicle JL: Pleiotropic effects on seed development of the
indeterminate gametophyte gene in maize. Amer J Bot 1971, 58:1-7.
43. Sheridan WF, Huang B-Q: Nuclear behavior is defective in the
•
maize (Zea mays L.) lethal ovule2 female gametophyte. Plant J
1997, 11:1029-1041.
A careful analysis of the mutant phenotype using fluorescent microscopy.
The results indicate that lethal ovule2 is essential for nuclear division, migration and the accompanying tubulin cytoskeleton behavior during maize
embryo sac development.
44. Ma H, Yanofsky MF, Meyerowitz EM: AGL1-ALG6, an Arabidopsis
gene family with similarity to floral homeotic and transcription
factor genes. Genes Dev 1991, 5:484-495.
45. Rounsley SD, Ditta GS, Yanofsky MF: Diverse roles for MADS
box genes in Arabidopsis development. Plant Cell 1995,
7:1259-1269.
46. Savidge B, Rounsley SD, Yanofsky M: Temporal relationship
between the transcription of two Arabidopsis MADS box genes
and the floral organ identity genes. Plant Cell 1995, 7:721-733.
47.
Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW:
Homeotic transformation of ovules into carpel-like structures in
Arabidopsis. Plant Cell 1994, 6:333-349.
48. Robinson-Beers K, Pruitt RE, Gasser CS: Ovule development in
wild-type Arabidopsis and two female-sterile mutants. Plant Cell
1992, 4:1237-1249.
49. Lang JD, Ray S, Ray A: sin1, a mutation affecting female fertility in
Arabidopsis, interacts with mod1, its recessive modifier. Genetics
1994, 137:1101-1110.