Arabidopsis thaliana outer ovule integument morphogenesis: Ectopic expression of KNAT1 reveals a compensation mechanism
BMC Plant Biology
Arabidopsis thaliana outer ovule integument morphogenesis: Ectopic expression of KNAT1 reveals a compensation mechanism
Elisabeth Truernit 0 1
Jim Haseloff 1
0 INRA, Centre de Versailles, Institut Jean-Pierre Bourgin, Laboratoire de Biologie Cellulaire , Route de St-Cyr, 78026 Versailles cedex , France
1 University of Cambridge, Department of Plant Sciences , Downing Site, Cambridge CB2 3EA , UK
Background: The Arabidopsis outer ovule integument is a simple two-cell layered structure that grows around the developing embryo and develops into the outer layer of the seed coat. As one of the functions of the seed coat is the protection of the plant embryo, the outer ovule integument is an example for a plant organ whose morphogenesis has to be precisely regulated. Results: To better characterise outer ovule integument morphogenesis, we have isolated some marker lines that show GFP expression in this organ. We have used those lines to identify distinct cell types in the outer integument and to demonstrate similarities between leaves and the outer integument. Using confocal microscopy, we showed that cell sizes and shapes differ between the two cell layers of the outer integument. Expression of KNAT1 in the integuments leads to extra cell divisions specifically in the outer layer of the outer integument. This is being compensated for by a decrease of cell volume in this layer, thus showing that mechanisms exist to control proper ovule integument morphogenesis. Conclusion: The Arabidopsis outer ovule integument can be used as a good model system to study the basic principles of plant organ morphogenesis. This work provides new insights into its development and opens new possibilities for the identification of factors involved in the regulation of cell division and elongation during plant organ growth.
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Background
Fertilised ovules develop into seeds that contain the plant
embryo. In Arabidopsis thaliana, three distinct regions can
be identified along the proximal-distal axis of the ovule
primordium (Figure 1). The most proximal structure of
the primordium is the funiculus, which connects the
primordium to the placenta. At the distal end of the
primordium lies the nucellus in which the megaspore mother cell
develops. The chalaza in the central zone of the
primordium initiates two integuments, each composed of two
cell layers [1,2]. During ovule development, the two
integuments grow around the nucellus and, after fertilization,
develop into the seed coat that encloses the embryo
(Figure 1). Whereas the inner integument initially develops as
a radially symmetrical structure that surrounds the
nucellus, the outer integument grows only from the side of the
ovule primordium that faces the basal end of the carpel
(gynobasal side) [1,2]. The outer integument remains
two-cell layered throughout seed development [1,2]. At
later stages of seed development, cells of the abaxial
(outer) layer of the outer integument differentiate
termiTFihgeudreev1elopment of ovule integuments in Arabidopsis
The development of ovule integuments in Arabidopsis. (A) Two inner and one outer integument grow out from the
chalaza (c) during early ovule development. (B) Ovule at stage of fertilization: Integuments have grown around nucellus (n),
i.i.1: inner (adaxial) layer of inner integument, i.i.2: outer (abaxial) layer of inner integument, o.i.1: inner (adaxial) layer of outer
integument, o.i.2: outer (abaxial) layer of outer integument.
nally into highly specialized seed coat cells that contain
polysaccharide mucilage [3,4].
The integuments are the only lateral organs produced by
the ovule. The evolutionary origin of the integuments is
still a matter of debate. The telome theory suggests that
integuments originated from the fusion of sterile or fertile
branches (telomes) [5,6]. It is generally believed that the
inner and outer integument derived independently. While
the inner integument most likely originated directly from
the fusion of telomes or sporangiophores, the outer
integument is believed to have developed later from a cupule,
a leaf-like structure surrounding one or more ovules [7,8].
The development of the Arabidopsis outer ovule
integument involves the same basic processes required for the
formation of other determinate lateral plant organs, such
as leaves. The outer ovule integument is an example for an
organ of determinate growth and characteristic form in
which the rate and direction of cell division and
elongation needs to be precisely regulated. Asymmetric growth
and differentiation are also essential features of its
development. In case of the integuments, proper
morphogenesis is especially critical, as an improper curvature or
closure would lead to seeds with embryos that are not
sufficiently protected. However, it seems that integument
extension is relatively sensitive to alterations in cell
division or cell expansion. Mutations in SHORT
INTEGUMENTS2 (SIN2), for example, lead to shorter
integuments du (...truncated)