Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008, Zurich, Switzerland
* Present address: Max-Planck Institut für Entwicklungsbiologie, Spemannstrasse 35, D-72076, Tübingen, Germany
Present address: Entwicklungsbiologie der Pflanzen, Wissenschaftszentrum Weihenstephan, Technische Universität München, Am Hochanger 4, 85354 Freising, Germany
Author for correspondence (e-mail: schneitz{at}wzw.tum.de)
Accepted 1 July 2002
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SUMMARY |
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Key words: Ovule development, Pattern formation, Organogenesis, Arabidopsis thaliana, NOZZLE, INNER NO OUTER
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INTRODUCTION |
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How are these patterns set up and what are the underlying molecular mechanisms? Genetic and molecular analysis have identified several genes that play a role in pattern formation along these two axes. BELL1 (BEL1) encodes a homeodomain protein and bel1 mutants show abnormal outgrowths in place of integuments (Modrusan et al., 1994a; Ray et al., 1994
; Reiser et al., 1995
; Schneitz et al., 1997
). BEL1 is expressed throughout the ovule primordia in the initial stages, but is restricted to the central region before the initiation of integuments, and thus marks the central region at a molecular level (Reiser et al., 1995
). The biochemical nature of the BEL1 protein, the expression pattern of BEL1 and the bel1 phenotype make BEL1 an excellent candidate for patterning the PD axis. Recently we have reported the genetic analysis of NOZZLE (NZZ) and shown that NZZ functions redundantly with BEL1 in specifying the chalaza (Balasubramanian and Schneitz, 2000
). In the ovules of nzz bel1 double mutants no chalaza structures are detectable and the tissue that is formed in the central region resembles funiculus as seen by the epidermal cell morphology. NZZ encodes a novel protein that plays a role in both male and female reproductive development (Balasubramanian and Schneitz, 2000
; Schiefthaler et al., 1999
; Yang et al., 1999
). NZZ shows an antagonistic genetic interaction with AINTEGUMENTA (ANT), which encodes an AP2 domain-containing transcription factor (Elliott et al., 1996
; Klucher et al., 1996
). ANT controls cell proliferation and organ size during ovule and flower development (Krizek, 1999
; Krizek et al., 2000
; Liu et al., 2000
; Mizukami and Fischer, 2000
; Schneitz et al., 1998
). From our previous genetic analysis of nzz, we proposed that NZZ, through its interactions with BEL1 and ANT, couples PD pattern formation and growth during ovule development in Arabidopsis thaliana (Balasubramanian and Schneitz, 2000
).
What regulates the Ad-Ab pattern formation? Studies in several species have identified many loci that regulate Ad-Ab patterning during lateral organ formation. Analysis of mutants like phantastica (phan) of Antirrhinum, leafbladeless (lbl1) of maize, lam1 of Nicotiana and argonaute (ago1), pinhead/zwille (pnh/zll), phabulosa (phb) and phavoluta (phv) of Arabidopsis have shown that the corresponding wild-type genes promote adaxial cell fate (Bohmert et al., 1998; Lynn et al., 1999
; McConnell and Barton., 1998
; McConnell et al., 2001
; McHale and Marcotrigiano, 1998
; Timmermans et al., 1998
; Waites and Hudson, 1995
). Contrary to this, the members of the YABBY gene family, which encode transcription factors, and the KANADI genes, which also encode transcription factors, promote abaxial cell fate (Bowman, 2000a
; Eshed et al., 1999
; Golz and Hudson, 1999
; Kerstetter et al., 2001
; Siegfried et al., 1999
). The members of the YABBY gene family are expressed in a polar manner at the abaxial side of lateral organs. KANADI genes redundantly promote abaxial cell fate possibly by negative regulation of the PHB/PHV mediated adaxial signaling. When KANADI function is compromised, adaxialised organs are formed (Eshed et al., 2001
).
INNER NO OUTER (INO), a member of the YABBY family plays a vital role in Ad-Ab pattern formation during ovule development (Villanueva et al., 1999). ino mutants exhibit ovules that lack the outer integument (Baker et al., 1997
; Schneitz et al., 1997
) and INO expression is detected in cells that give rise to the outer integument before its initiation (Villanueva et al., 1999
). Therefore, it has been implicated in the establishment and maintenance of this axis in ovules. SUPERMAN (SUP), a gene that encodes a zinc finger transcription factor, is another locus that regulates the Ad-Ab pattern formation (Gaiser et al., 1995
; Sakai et al., 1995
). Interestingly in sup mutants, the outer integument initiates properly, but grows equally on both adaxial and abaxial side suggesting that SUP may be necessary for the maintenance rather than the initial establishment of the Ad-Ab axis.
The orchestration of cell activities along the various axes of polarity is crucial for the proper development of any organ. How is the co-ordination of cell activities along the PD and Ad-Ab axis achieved during ovule development? What is the molecular link between patterning along these two axes? How is the expression of INO regulated in a spatial and temporal manner to ensure that such a co-ordination is achieved? Here we report the expression patterns of INO in various mutant backgrounds and show how its transcription is regulated in a spatial and temporal manner. We show that the co-ordination of BEL1, ANT and NZZ activities is required for the onset and temporal expression of INO. We show that at least three genes NZZ, ATS and SUP regulate the spatial expression of INO. We present evidence that NZZ and ATS spatially restrict the expression of INO to the abaxial epidermis. We further report the expression patterns of ANT in ino and nzz ino double mutants and show that the positive auto-regulatory control of INO expression (Villanueva et al., 1999) involves ANT. We propose a model that summarises our findings and explains how Ad-Ab patterning and outer integument development occurs during ovule development in Arabidopsis. Our analysis indicates NZZ as a molecular link that orchestrates pattern formation along PD and Ad-Ab axis during ovule development in Arabidopsis.
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MATERIALS AND METHODS |
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Scanning electron microscopy (SEM) and in situ hybridisation
SEM and image processing has been described previously (Balasubramanian and Schneitz, 2000; Schiefthaler et al., 1999
; Schneitz et al., 1998
; Schneitz et al., 1997
). The protocol for in situ hybridisation and the INO, BEL1 and ANT probes that were used in these experiments have also been described previously (Balasubramanian and Schneitz, 2000
). In situ experiments were repeated several times, with different batches of fixed material to rule out the possibility of a negative result due to experimental or material batch differences. Furthermore, the sections of wild-type and the mutant tissues were processed together in order to minimise experimental differences.
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RESULTS |
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Expression patterns of INO in wild type, ant-72F5, ino-2 and bel1-1460
Mutations in the INO locus lead to lack of the outer integument (Baker et al., 1997; Schneitz et al., 1997
). INO expression can be detected in cells that will give rise to the outer integument, before its initiation, and therefore it is the earliest molecular manifestation of the Ad-Ab polarity (Villanueva et al., 1999
). ino exhibits complex genetic interactions and several putative regulators of INO expression have been reported. BEL1, ANT, HUELLENLOS (HLL) and SUP were suggested to be negative regulators of INO expression (Villanueva et al., 1999
). In contrast, we have previously reported the absence of INO expression in bel1-1460 and ant-72F5 mutants at about stage 2-II (Balasubramanian and Schneitz, 2000
). In order to understand the regulation of INO expression and outer integument development, we undertook to analyse INO expression in wild type and various mutants during various stages of ovule development.
Expression of INO during wild-type ovule development
INO expression could be first detected at about stage 2-I (Fig. 2B). Around stage 2-III, when the outer integument initiation becomes visible, INO expression is observed in the epidermal cells that enlarge (Fig. 2C). Interestingly, the cell that undergoes cell division to give rise to the triangular tip cell and subsequently the two cell layers, does not express INO (Fig. 2C arrow). Later during development, INO expression is observed only in about 3-4 cells at the distal end of the abaxial cell layer of the outer integument. The adaxial cell layer of the outer integument does not show any INO expression (Fig. 2D).
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Expression of INO during ovule development in nzz-2, ats, sup and nzz-2 ats
We tested if the differences that we observed in the outer integument development in nzz-2 ats double mutants were reflected in a change in INO expression by analysing its expression in nzz-2, ats and nzz-2 ats mutant backgrounds. In nzz-2, the expression of INO was detected at the site of outer integument, before its initiation (Fig. 3A). The outer integument initiates earlier in nzz mutants (Fig. 1F), suggesting precocious INO expression in nzz. With respect to the Ad-Ab axis, the expression of INO in nzz-2 showed no deviation from wild type (Fig. 3B-D). In addition, INO expression could easily be detected with shorter colour reaction times (about 12 hours) in nzz-2 compared to wild type (about 36 hours) hinting at an increased level of INO expression in nzz-2. In ats mutants, INO expression followed a wild-type expression pattern (Fig. 3E,F). In contrast to the single mutants of both nzz-2 and ats, nzz-2 ats double mutants showed drastic alterations in the expression pattern of INO during ovule development. At initial stages, the normal INO expression pattern was observed, though a weak signal was detected throughout the central region (Fig. 3Ia). Sometimes, it was more obvious, with INO expression detected throughout the central region similar to a BEL1 or ANT stripe (Fig. 3Ib). This was even more pronounced at around stage 2-III and all the ovules that we observed (n>40) showed the expression of INO throughout the central region (Fig. 3J). Later, INO expression was detected on both the adaxial and the abaxial side of the ovule and in both the adaxial and abaxial cell layers of the outer integument (Fig. 3K). Even around stage 3-IV, INO expression was detected throughout the central region and was not restricted to the epidermis (Fig. 3La). The misexpression of INO in the central region was also reported in sup-5 mutants (Villanueva et al., 1999). In sup-5 mutants, the initial onset of INO expression was unaltered (Fig. 3G) but the subsequent expression of INO is similar to that seen in nzz-2 ats double mutants (compare Fig. 3H and J).
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DISCUSSION |
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NZZ and ANT are temporal regulators of INO expression
Our analysis of the expression pattern of INO in ant and nzz indicates that the proper temporal expression of INO requires co-ordination of ANT and NZZ activities. nzz mutants show early initiation of the outer integument, which is preceded by the expression of INO, suggesting that NZZ is a negative temporal regulator of INO expression. In contrast to this, ant mutants show late onset of INO expression (Fig. 2H), suggesting that ANT is a positive temporal regulator of INO expression. ANT and NZZ act antagonistically in all regions of the ovule (Balasubramanian and Schneitz, 2000). The presence of INO, at later stages, in the strong ant-72F5 mutant suggests that ANT is not absolutely required to turn on INO, rather ANT may be needed for the proper timing of INO expression. Taken together, these data suggest that the proper temporal expression of INO requires co-ordination of NZZ and ANT activities. Our analyses suggest a possible increase in the level of INO expression in nzz mutants. The antagonistic interaction of NZZ and ANT also leaves open the possibility that the expression of INO might equally well depend on the relative levels of ANT and NZZ activity. This negative regulation of INO by NZZ could be an essential temporal mechanism to couple PD patterning with Ad-Ab patterning (see below)
NZZ and ATS redundantly regulate INO expression and play a role in the maintenance of the adaxial-abaxial polarity
If ANT and NZZ regulate the temporal expression of INO, what regulates its spatial expression? Previously several loci were reported as negative regulators of INO expression (Villanueva et al., 1999). As we have shown above, ANT and BEL1 are positive regulators of INO expression. Contrary to this, NZZ acts as a negative regulator of INO, not only in a temporal manner but also in a spatial manner. Our analysis shows that NZZ and ATS redundantly negatively regulate INO expression in the adaxial chalaza (Fig. 3I-L). Any one of these loci is sufficient to restrict INO expression to the abaxial side since ats or nzz single mutants show normal abaxially located INO expression. How do NZZ and ATS regulate INO expression? We suggest at least two possibilities. First, NZZ and ATS are general negative regulators of INO expression and this inhibition is specifically overcome in the abaxial epidermis with the help of other factors such as ANT. The broad expression pattern of NZZ in the ovules (Balasubramanian and Schneitz, 2000
; Schiefthaler et al., 1999
) and the expression pattern of ANT in nzz mutants support such a hypothesis. The absence of the ANT spot in nzz ino double mutants also supports this hypothesis. In nzz ats, the negative regulation by NZZ and ATS is absent and INO is expressed throughout the central region. Alternatively, NZZ and ATS might play a role only in the negative regulation of INO expression in the adaxial region. Is NZZ and ATS function required for initiation of the Ad-Ab axis or its maintenance? From our analysis it is clear that NZZ and ATS are definitely required for its maintenance. However, the weak misexpression of INO even in stage 2-I ovules of nzz ats double mutants suggests that they may play a role in the initiation of this axis as well. Why then is this misexpression weak at initial stages? It is possible that the ats allele available could be a weak allele. Since the molecular nature of ATS is not known, the nature of the ats allele is not clear.
NZZ, ATS, INO and SUP play a role in the asymmetric growth of the outer integument
INO and SUP have been previously reported to mediate the asymmetric growth of the outer integument (Gaiser et al., 1995; Schneitz et al., 1997
; Villanueva et al., 1999
). Our analysis of nzz ats double mutants indicates that NZZ and ATS are also required for the control of the asymmetric growth of the outer integument. Spatially, the ovules of nzz ats double mutants show no alterations in the initiation of the outer integument along the adaxial-abaxial axis. This indicates that NZZ and ATS are likely to play a role in the asymmetric growth of the outer integument after its initiation. Nevertheless, the altered expression pattern of INO at the initial stages itself in nzz ats (Fig. 3Ib) suggests that NZZ and ATS might also play a role in specifying this axis (see above). Since the single mutants of nzz and ats do not show any alterations in the asymmetric growth, we conclude that NZZ and ATS redundantly regulate the asymmetric growth of the outer integument.
SUP, NZZ and ATS are required for the maintenance of the adaxial-abaxial polarity during ovule development
SUP is another locus that regulates INO expression in the adaxial region of the chalaza. SUP has been suggested to be a negative regulator of INO expression (Villanueva et al., 1999). Our analysis of INO expression in sup mutants corroborates this hypothesis. The broader expression pattern of INO in sup mutants around stage 2-III is similar to that observed in nzz ats double mutants. How then does SUP relate to NZZ and ATS? Currently this remains an open question. However, we suggest at least three possibilities. First, NZZ and ATS function redundantly upstream of SUP. Second, SUP functions upstream of NZZ and ATS. Third, NZZ, ATS and SUP function at the same step of the cascade, in which case, SUP would be the central player. A genetic analysis of nzz sup double mutants did not allow us to discriminate between these possibilities as these mutants show sup-like ovules that lack the nucellus and thus exhibit an additive phenotype (data not shown). The observation that at least in some instances the INO expression is altered even at initial stages in nzz ats double mutants, suggests that NZZ and ATS might function earlier than SUP.
Outgrowth of the outer integument might require proper juxtaposition of the adaxial-abaxial signals
Why do the ino mutants produce ovules that lack the outer integument? It has been suggested that in ino mutants adaxialisation of the abaxial side of the outer integument leads to minimal or no outgrowth (Villanueva et al., 1999). Based on our analysis of wild-type INO expression, we propose a hypothesis to explain why adaxialisation should stop the outgrowth? Genetically ino is epistatic to sup, nzz and ats with respect to the outer integument, which fits well with the hypothesis that INO may be required for the initial outgrowth of the outer integument. As we have shown above, the tip cell, which usually enlarges and initiates the outgrowth, does not express INO. Then why should the absence of INO prevent the outgrowth? It has been suggested that juxtaposition of adaxial and abaxial signals may be needed for the outgrowth of lateral organs, similar to the requirement of dorsal and ventral signals during lateral appendage development in animals (Bowman, 2000b
; Waites and Hudson, 1995
). It is possible that in ino mutants such a juxtaposition of the adaxial and abaxial signals within the outer integument is not achieved because of the absence of INO. This fits well with the observation that INO expression is observed in only one cell layer of the outer integument and the absence of INO expression from the tip cell that enlarges to give rise to the outer integument. We suggest that the outgrowth of the outer integument requires proper juxtaposition of the adaxial and abaxial signals within the outer integument itself, which could be the reason why ino mutants lack the outer integument.
A model for outer integument development and regulation of INO expression
Our results are summarised in Table 1 and we propose a model that attempts to explain the genetic regulation of adaxial-abaxial pattern formation and outer integument development during ovule development (Fig. 5). NZZ plays a central role in different aspects of ovule development and it is required repeatedly during various stages of ovule development. We have previously proposed that NZZ and BEL1 redundantly specify the chalaza (Balasubramanian and Schneitz, 2000). Furthermore, with respect to the integument development pathway, NZZ functions downstream of ANT and INO (Balasubramanian and Schneitz, 2000
). In the model that we propose here, we suggest that initiation of the outer integument and Ad-Ab polarity establishment in the ovule occur after specification of the chalaza. This is achieved at least in part through the co-ordination of activities of ANT, BEL1, NZZ, ATS and SUP. The exact positioning of INO expression in the abaxial epidermis of the proximal chalaza may require other factors as well. Once INO is turned on, maintenance of its expression goes through an auto-regulatory loop that includes ANT. Subsequent ANT expression has a positive feedback on INO as well as NZZ. How does INO regulate NZZ expression? If INO regulates ANT via NZZ, then one would not detect increased levels (spot) of ANT in nzz mutants. Therefore, it is likely that the positive feedback regulation of ANT by INO is separate from the negative feedback of NZZ on ANT (Fig. 5B), though these two regulations are inter-connected. Thus, the positive feedback of INO on ANT leads to a positive regulation of NZZ by ANT. NZZ in turn has a negative feedback on ANT. In the adaxial side, NZZ redundantly regulates INO expression with ATS. This could be mediated via SUP or could be exerted independently (see above). If this model is true, then what would happen in a nzz mutant? In the absence of NZZ, INO is turned on precociously. Once INO is turned on, it leads to a positive feedback on ANT expression and consequently an increase in INO expression as well. This would also lead to an increase in NZZ expression in the outer integument. Since the NZZ protein is nonfunctional in nzz-2, this will lead to increased levels of ANT and INO. The predictions of this model hold true at least for ANT expression in nzz-2. nzz-2 mutants show an increased expression of ANT in the cells that give rise to the outer integument. This model is also supported by the fact that INO expression can be detected more easily in nzz-2 than in wild type. Furthermore, this model also supports the absence of the ANT spot in nzz ino double mutants.
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ACKNOWLEDGMENTS |
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