- Review
Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex
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Fig. 1.
Adaxial-abaxial leaf architecture. (A) The adaxial side of an
Arabidopsis leaf is dark green and trichome rich, whereas the abaxial
leaf surface is matte, grey-green and trichome poor. (B) The adaxial
and abaxial sides of a maize leaf blade (b) and sheath (s) are separated by
the auricle (a) and the ligule (l), an adaxial, epidermal fringe. (C)
Transverse section of an Arabidopsis leaf, showing adaxial palisade
cells (p), abaxial spongy mesophyll cells (s) and the central midvein (mv).
(D) Magnified cross-section of a vascular bundle in an
Arabidopsis leaf, showing the spatial relationship between adaxial
xylem (x) and abaxial phloem (ph). Images C and D, which were first published
by Lin et al. (Lin et al.,
2003), are reproduced with permission from the American Society of
Plant Biologists.
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Regulating Proxima-Distal and Adaxial-Abaxial Patterning during early Ovule Development.
Ovules are the major female reproductive organs of
higher plants. Within the ovule the egg cell is produced and, upon
fertilisation, the embryo develops during seed development. Arabidopsis
ovules provide an excellent system to study pattern formation and
aspects of organ polarity establishment in plants (Schneitz et al.,
2001, Gasser et.al., 1998). Ovules develop from the placenta inside
gynoecia as finger-like protrusions. Three proximal-distal elements, the
funiculus, chalaza and nucellus, can be distinguished early on (Esau,
1977; Schneitz et al., 1995). Within the distally-located nucellus
meiosis takes place in the megaspore mother cell. Only one of the four
megaspores survives and develops into the multicellular, haploid female
gametophyte, the embyro sac. One of the cells of the embryo sac is the
egg cell proper. The chalaza is located beneath the nucellus and is
characterised by the two integuments, the progenitors of the seed coat,
inititating from its flanks. The funiculus is a stalk-like structure,
which harbors the vascular strand and connects the ovule to the
placenta.
After the primordium completed its proximal-distal
extension the inner and outer integuments develop in a sequential
fashion. First, the inner integument initiates as a collar around the
chalaza. Second, the outer integument initiates but first on the
gynbasal side of the primordium, which is the side towards the base of
the gynoecium. Outer integument initiation at the chalaza is the first
morphological evidence that adaxial-abaxial polarity establishment had
has occurred and that the radially symmetrically primordium had has
switched to bilateral development (Baker et al., 1997).
Some progress has recently been made towards the
understanding of the molecular mechanism underlying the coordination of
proximal-distal and adaxial-abaxial pattern formation. At least two
genes, NOZZLE (NZZ) and INNER NO OUTER (INO), appear to be essential for this aspect of pattern formation. Before the integuments initiate, transcription of INO can be detected in a few cells on the abaxial side of the ovule. Developing ovules lacking INO
function only form the inner integument and thus appear radialized
(Balasubramanian and Schneitz, 2000; Balasubramanian and Schneitz, 2002;
Meister et al., 2002; Villanueva et al., 1999). INO belongs to the
YABBY family of putative plant-specific transcription factors
(Villanueva et al., 1999). Additional members include FIL and YABBY3
(YAB3) (Bowman, 2000). YABBY genes are associated with the
regulation of abaxial cell fate by a mechanism which presently is not
understood (reviewed in Bowman et al., 2000; Bowman and Smyth, 1999;
Eshed et al., 1999; Sawa et al., 1999; Siegfried et al., 1999;
Villanueva et al., 1999). There is evidence coming from in vitro binding
studies, that FIL protein dimers bind to DNA through their high
mobility group (HMG)-like (YABBY) domains in a non-sequence-specific
fashion (Kanaya et al., 2002).
We have recently identified the NZZ gene (Schiefthaler et al., 1999), also known as SPOROCYTELESS (SPL) (Yang et al., 1999). NZZ encodes a novel protein which is likely to be a putative transcriptional regulator. Extensive genetic evidence indicates that NZZ
coordinates development of the proximal-distal and adaxial-abaxial axes
to allow proximal-distal axis formation before the initiation of the
adaxial-abaxial axis and outer integument development in the chalaza
(Balasubramanian and Schneitz, 2000; Balasubramanian and Schneitz,
2002). NZZ appears to control INO expression in a temporal fashion via its negative regulation of the positive auto-regulatory loop of INO
transcription (Balasubramanian and Schneitz, 2000; Balasubramanian and
Schneitz, 2002; Meister et.al., 2002). Biochemical in vitro studies
indicate that the NZZ protein can directly bind to INO, thereby
inhibiting INO function and attenuating the INO feedback loop (Sieber
et.al., 2004). We are presently continuing to elucidate the
corresponding molecular mechanism.
References
Balasubramanian, S. and Schneitz, K. (2002). NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129, 4291-4300.
Balasubramanian, S. and Schneitz, K. (2000). NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis in Arabidopsis thaliana. Development 127, 4227-4238.
Bowman, J. L. and Smyth, D. R. (1999). CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126, 2387-2396.
Bowman, J. L. (2000). The YABBY gene family and abaxial cell fate. Curr. Opin. Plant Biology 3, 17-22.
Bowman, J. and Eshed, Y. (2000). Formation and maintenance of the shoot apical meristem. Trends in Plant Science 5, 110-115.
Esau, K. (1977). Anatomy of Seed Plants. New York: John Wiley & Sons.
Eshed, Y., Baum, S. F. and Bowman, J. L. (1999). Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199-209.
Gasser, C. S., Broadhvest, J., and Hauser, B. A. (1998). Genetic analysis of ovule development. Annu Rev Plant Physiol Plant Mol Biol 49, 1-24.
Kanaya, E., Nakajima, N. and Okada, K. (2002). Non-sequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA. J Biol Chem 277, 11957-11964.
Meister, R. J., Kotow, L. M., and Gasser, C. S. (2002). SUPERMAN attenuates positive INNER NO OUTER autoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 129, 4281-4289.
Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Hayato Morita, E. and Okada, K. (1999). FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088.
Sieber, P., Petrascheck, M., Barberis, A. and Schneitz, K. (2004). Organ polarity in Arabidopsis. NOZZLE physically interacts with members of the YABBY family. Plant Physiology 135: 2172-2185.
Siegfried, K. R., Eshed, Y., Baum, S. F., Otsuga, D., Drews, G. N. and Bowman, J. L. (1999). Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117-4128.
Villanueva, J. M., Broadhvest, J., Hauser, B. A., Meister, R. J., Schneitz, K. and Gasser, C. S. (1999). INNER NO OUTER regulates abaxial/adaxial patterning in Arabidopsis ovules. Genes Dev. 13, 3160-3169.
Yang, W.-C., Ye, D., Xu, J. and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108-2117.
Balasubramanian, S. and Schneitz, K. (2002). NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129, 4291-4300.
Balasubramanian, S. and Schneitz, K. (2000). NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis in Arabidopsis thaliana. Development 127, 4227-4238.
Bowman, J. L. and Smyth, D. R. (1999). CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126, 2387-2396.
Bowman, J. L. (2000). The YABBY gene family and abaxial cell fate. Curr. Opin. Plant Biology 3, 17-22.
Bowman, J. and Eshed, Y. (2000). Formation and maintenance of the shoot apical meristem. Trends in Plant Science 5, 110-115.
Esau, K. (1977). Anatomy of Seed Plants. New York: John Wiley & Sons.
Eshed, Y., Baum, S. F. and Bowman, J. L. (1999). Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199-209.
Gasser, C. S., Broadhvest, J., and Hauser, B. A. (1998). Genetic analysis of ovule development. Annu Rev Plant Physiol Plant Mol Biol 49, 1-24.
Kanaya, E., Nakajima, N. and Okada, K. (2002). Non-sequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA. J Biol Chem 277, 11957-11964.
Meister, R. J., Kotow, L. M., and Gasser, C. S. (2002). SUPERMAN attenuates positive INNER NO OUTER autoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 129, 4281-4289.
Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Hayato Morita, E. and Okada, K. (1999). FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088.
Sieber, P., Petrascheck, M., Barberis, A. and Schneitz, K. (2004). Organ polarity in Arabidopsis. NOZZLE physically interacts with members of the YABBY family. Plant Physiology 135: 2172-2185.
Siegfried, K. R., Eshed, Y., Baum, S. F., Otsuga, D., Drews, G. N. and Bowman, J. L. (1999). Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117-4128.
Villanueva, J. M., Broadhvest, J., Hauser, B. A., Meister, R. J., Schneitz, K. and Gasser, C. S. (1999). INNER NO OUTER regulates abaxial/adaxial patterning in Arabidopsis ovules. Genes Dev. 13, 3160-3169.
Yang, W.-C., Ye, D., Xu, J. and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108-2117.
Fachgebiet Entwicklungsbiologie der Pflanzen
TU MünchenEmil-Ramann-Str. 4
85354 Freising
Germany
Tel.: +49 8161 / 71 5438
Fax: +49 8161 / 71 3337
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