Journal of Experimental Botany, Vol. 53, No. 377, pp. 2031-2038,
October 1, 2002
© 2002 Oxford University Press
Regulation of fruit dehiscence in Arabidopsis
Received 26 March 2002; Accepted 5 July 2002
Instituto de Biología Molecular y Celular de Plantas, CSIC, Campus de la Universidad Politécnica de Valencia, Av. de los Naranjos, 46022 Valencia, Spain
1 Fax: +34 96 387 7859. E-mail: cferma{at}upvnet.upv.es
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Abstract |
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 Top Abstract IntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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Fruit dehiscence is a strategy that many fruits adopt to achieve seed dispersal. The dehiscence process involves the differentiation of specialized cell types and a tight co-ordination of molecular and biochemical events that eventually lead to a cell separation process that frees the seeds once they have matured. In the last few years, great progress has been made in identifying the molecular mechanisms underlying fruit dehiscence in the model plant Arabidopsis thaliana. In this review, a summary of our current knowledge is presented, and possible future explorations are suggested.
Key words: Key words: Arabidopsis, fruit dehiscence, regulation.
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Introduction |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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Fruits have evolved to mediate the maturation and dispersal of seeds. For this purpose, a multitude of mechanisms can be found. Essentially, the fruit is a mature ovary, which may include additional parts of the flower, forming a complex structure that can be arranged in a great variety of ways. Among these, many dry simple fruits undergo a process of dehiscence to achieve seed dispersal. This process is accomplished through a carefully orchestrated event that occurs late in fruit development, and involves the differentiation of specialized cell types that must allow cell separation at some point.
Since the manipulation of dehiscence could improve crop yield, both plant breeders and scientists have focused their attention on this process. Physiological studies from the 1970s focused on fruits such as cotton and pecan (Lipe and Morgan, 1972), while in the last decade, Brassica napus became the focus for the morphological and molecular characterizations of the dehiscence process (Meakin and Roberts, 1990a, b; Roberts et al., 2000). Comparative anatomical and physiological studies in the model plant Arabidopsis thaliana revealed that dehiscence is very similar to the same process in Brassica (Spence et al., 1996). The use of Arabidopsis, for which extensive genetic and molecular tools are available, has allowed a rapid advance in understanding how this process is regulated. In this review, the focus will be on the genetic mechanisms underlying the regulation of pod dehiscence in this model plant.
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The dehiscence process |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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The Arabidopsis fruit develops from a gynoecium composed of two fused carpels, which, upon fertilization, grows to become a typical silique that contains the developing seeds. After seed maturation, dehiscence takes place, and valves detach from the central septum freeing the seeds (Bowman et al., 1999; Ferrándiz et al., 1999; Fig. 1)
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The dehiscence zone (DZ) is a region that is no more than a few cells wide extending the entire length of the fruit at the boundaries between the valves and the replum (i.e. external septum). At maturity, the DZ can be considered to consist of a non-lignified separation layer (SL), placed between a region of lignified cells in the valve and the lignified vasculature of the replum (Fig. 1).
The differentiation of specialized tissues in the fruit is apparent from floral developmental stages 11/12 in Arabidopsis (according to Smyth et al., 1990), which is shortly before fertilization of the ovules. After fertilization (stage 13), longitudinal creases, corresponding to SL differentiation, clearly delimit the valves from the replum. Cells at the SL are morphologically different from adjacent non-separating cells. The SL cells differentiate early during silique development as small, isodiametric cells with dense cytoplasm and many plasmodesmatal connections, and appear to remain in a state of arrested development while the adjacent cells continue to differentiate, expand, and vacuolate. Cells of the inner epidermis of the valves (ena, according to Spence et al., 1996) expand and remain thin-walled, whereas cells of the inner subepidermal layer (enb) develop thickened walls (stage 17A, Ferrándiz et al., 1999), which subsequently lignify (stage 17B). Patches of a few mesocarp cells adjacent to the SL also become lignified (stage 17B). Simultaneously, the main vascular strands that run along the replum enlarge and show much additional lignification. Yellowing and desiccation of all tissues occurs, and cells of ena finally disintegrate (stage 18). During the final stages of fruit development, detachment of the valves from the replum proceeds (stage 19). Cell separation takes place by degradation of the middle lamella at the fracture surface of the SL. Spence et al. (1996) describe the cells at the SL as remaining intact. However, studies in Brassica napus by Meakin and Roberts (1990b) and the more recent work from Rajani and Sundaresan (2001) in Arabidopsis, support the idea that autolysis of SL cell protoplasts also takes place and could be needed for the release of cell-wall-degrading enzymes. Pod shatter appears to occur by a combination of cell wall loosening at the SL and the tensions established by the differential mechanical properties of the lignified tissues at the enb layer and the valve margin patches, and of the drying exocarp and mesocarp cells (Meakin and Roberts, 1990a; Spence et al., 1996).
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The genetics of pod shattering |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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In the last few years, many genes have been identified that are involved in DZ differentiation and in the associated biochemical and physiological changes prior to cell separation. Genes have been isolated through several different approaches. The identification of mutants both through classical mutagenesis and reverse genetics has led to the molecular cloning of genes that direct DZ cell differentiation (Liljegren et al., 2000a; Rajani and Sundaresan, 2001). An alternative strategy with valuable results has been the identification of genes specifically expressed in the DZ. Given the anatomical and physiological specificity of this tissue, genes that are specifically expressed in these cells and not in the valves are likely to be involved in dehiscence. In Brassica, DZ genes have been identified mainly by isolating mRNAs expressed in the valve margins (Coupe et al., 1993, 1994; Petersen et al., 1996; Whitelaw et al., 1999). This direct isolation is more difficult in Arabidopsis due to the smaller size of the silique, but the identification of Arabidopsis sequences related to Brassica DZ genes has revealed that sequence homology often correlates with expression pattern similarity (Jenkins et al., 1999; Sander et al., 2001). In the last few years, different laboratories have generated collections of Arabidopsis enhancer or gene trap lines. These experiments are based on the random insertion of reporter genes in the Arabidopsis genome, so that when inserted in the proximity of an enhancer or within a gene, the expression of the reporter is driven by the neighbouring regulatory sequences (Sundaresan et al., 1995). Several of these lines showing reporter expression in the valve margins have allowed the cloning of new DZ-related genes and the identification of different cell identities within the valve margin.
A variety of activities are required for pod shattering to occur. First, early regulators of cell differentiation must act to mediate cell fate specification. Once the different cell types are determined, then several enzymatic activities must work to accomplish the associated processes, such as changes in cell wall composition, lignification, and disintegration of the middle lamella in the separation layer. This programme of differentiation and the downstream enzymatic activities must be tightly regulated; therefore the signalling mechanisms are important to ensure a perfect co-ordination of events.
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The regulation of DZ cell differentiation |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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The first transcription factors shown to participate in DZ specification were the MADS-box genes SHATTER PROOF1 (SHP1) and SHATTERPROOF2 (SHP2). SHP1 and SHP2 are required for the proper specification of the different cell types within the valve margin and the DZ. They encode redundant activities, as the single mutants show no phenotype and only the double shp1 shp2 mutant siliques are unable to shatter after fruit desiccation. In shp1 shp2 siliques, lignification is reduced at the valve margins and the SL does not develop properly (Liljegren et al., 2000a). SHP1 and SHP2 probably represent the top of the hierarchy regulating DZ formation. They appear to be direct targets of regulation by AGAMOUS, a carpel identity gene, and their identical patterns of expression are restricted to cells that mark the DZ formation from very early stages in carpel development (Flanagan et al., 1996; Savidge et al., 1995).
Another MADS-box gene involved in dehiscence zone formation is FRUITFULL (FUL). FUL expression appears at the inception of the carpel primordia, and soon after becomes restricted to the cells that will give rise to the valves, a pattern that is complementary to that of the SHP genes (Gu et al., 1998; Mandel and Yanofsky, 1995). In ful mutants, the valves fail to elongate and differentiate after fertilization, the mesocarp cells lignify ectopically, and the valves usually tear open in what could be interpreted as the development of an ectopic DZ cell fate throughout the valve (Gu et al., 1998; Liljegren et al., 2000a). FUL negatively regulates the SHP genes in the valves, as the SHP genes become ectopically expressed in the valves of ful loss-of-function mutants. Conversely, fruits from plants constitutively expressing FUL are indehiscent due to a complete lack of DZ differentiation with conversion of all cells into a valve cell identity (Ferrándiz et al., 2000). This phenotype is somehow more severe that the shp1 shp2 phenotype, suggesting that FUL is probably not only acting through SHP repression, but also able to regulate other factors involved in DZ cell fate specification. It is interesting to note that, in addition to the SHP genes and FUL, other MADS-box genes appear to be involved in related processes of cell separation. For example, preliminary results indicate that the SEEDSTICK (STK) MADS-box gene is required for normal funiculus development and seed abscission and acts redundantly with SHP1 and SHP2 in repressing FUL in ovules and seeds (Pinyopich et al., 2001). Other examples are JOINT LESS, a tomato MADS-box gene required for the differentiation of the floral pedicel abscission zone (Mao et al., 2000; Szymkowiak and Irish, 1999), or AGL15, whose constitutive expression is able to prevent floral organ abscission (Fernandez et al., 2000).
A new element in DZ differentiation was identified by a gene trap line, GT140, that showed specific reporter expression in the valve margins of developing siliques (Sundaresan et al., 1995). GT140 reporter expression in the DZ was shown to be positively regulated by the SHP genes, and negatively regulated by FUL (Ferrándiz et al., 2000; Liljegren et al., 2000a). GT140 corresponds to a bHLH transcription factor, INDEHISCENT1 (IND1). IND1 is required for DZ differentiation, as loss-of-function ind1 mutant siliques lack the lignified patches at the valve margins and are unable to shatter. IND1 ectopic expression in ful mutant valves appears to be responsible for most of the ful phenotypes in the fruit, since ind1 mutations are largely able to suppress these phenotypes (Liljegren et al., 2000b; CF Yanofsky, M Yanofsky, unpublished results).
Recently, a new indehiscent mutant, alcatraz (alc) has been isolated. In alc mutants both lignification patterns and external morphology of DZ are normal, but close inspection reveals that alc SL fails to define a clear fracture layer. In the final stages of fruit development, lignified cells form a bridge between the enb layer and the vascular bundle of the replum, blocking valve detachment after middle lamella disintegration. ALC corresponds to another bHLH transcription factor and it is expressed preferentially in the valve margin, albeit with a dynamic pattern, becoming progressively restricted to the cells that form this lignified bridge in later stages (Rajani and Sundaresan, 2001). It is still unclear how ALC is regulated. SHP1, SHP2 and FUL levels of expression appear unchanged in the alc background, suggesting that ALC could be a downstream target of these genes, although further analysis needs to be done. alc ful double mutants show a partial reduction of ful phenotypes in the valves, suggesting that ALC might be repressed by FUL in this tissue, in a similar way to that observed for the SHP genes or IND1 (Rajani and Sundaresan, 2001).
Other candidate factors appear to be involved in DZ differentiation. One of these could be the gene corresponding to another gene trap line, YJ161. The YJ161 reporter is expressed in the inner and outer epidermis of the valve margin. This expression pattern is different from those of the SHP or IND1 genes, which span all cell layers of the valve margin, or the dynamic pattern of the ALC gene. The YJ161 valve margin expression is not regulated by SHP, but is negatively regulated by FUL. The YJ161 marker corresponds to the expression pattern of a putative zinc finger protein, for which future identification of loss-of-function mutants could provide new insights on DZ specific cell type differentiation (Roeder et al., 2001).
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The downstream effectors |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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Breakdown of the cell wall and, in particular, of the middle lamella, is a basic event in the process of dehiscence (see above), and a shared feature with other processes such as abscission or senescence (Patterson, 2001; Roberts et al., 2000). Cell wall loosening proceeds through the action of extracellular enzymes such as cellulases and pectinases. Several of these enzymatic activities can be recognized in Arabidopsis, and it appears that some of those involved in dehiscence are specific to this process.
The first gene cloned that has been shown to be related to pod shattering encodes a polygalacturonase (PG), an enzyme responsible for degradation of the major component of pectin, expressed in the DZ of Brassica napus pods (SAC66, Jenkins et al., 1996; RDPG1, Petersen et al., 1996). A homologous gene in Arabidopsis was isolated by these two groups, based on high sequence similarity in both the regulatory and the coding regions, (SAC70, Jenkins et al., 1999; ADPG1, Sander et al., 2001). Detailed expression pattern analyses have been performed in heterologous systems, both by examining RDPG1 promoter activity in Arabidopsis transgenic plants (Sander et al., 2001), and SAC70 promoter activity in Brassica (Jenkins et al., 1999). In Brassica, the SAC70 promoter drives reporter expression in cells of the DZ that will undergo separation. Interestingly, SAC70 expression was also detected in regions where two other processes of cell separation occur: in the junction between the seed and the funiculus prior to seed abscission, and in cells adjacent to the anther dehiscence site. Similar results were observed when SAC70 promoter activity was tested in Arabidopsis (Roberts et al., 2002). In addition to transcriptional regulation, a post-translational control of PG activity has been proposed. RDPG1, and other PGs expressed in fruit, dehiscence and abscission zones, have a cleavable N-terminal domain. The presence of this N-terminal peptide appears to block PG secretion into the cell wall, and only upon its removal, triggered by an unknown signal, is the mature protein directed to the extracellular compartment to exert its function (Dal Degan et al., 2001).
An increase in ß-1,4-glucanase (cellulase) activity has been reported during Brassica napus pod dehiscence, although the corresponding gene has yet to be identified (Meakin and Roberts, 1990b). In plants, ß-1,4-glucanases have tissue-specific patterns of expression associated with many developmental processes such as tissue expansion, fruit ripening or organ abscission (Brummell and Harpster, 2001). In the Arabidopsis genome, several putative cellulases can be recognized (Henrissat et al., 2001). Whether the ß-1,4-glucanase activity involved in dehiscence is specific to this process or not needs to be clarified and the corresponding gene(s) identified.
Another enzymatic activity related to wall loosening is xyloglucan endotransglycosylase (XET) (Fry et al., 1992). An XET-encoding gene is specifically up-regulated in the DZ of Brassica napus at the final stages of pod development (Roberts et al., 2000). In Arabidopsis, an enhancer trap line was identified (YJ8) which has a T-DNA inserted 
3 kb upstream of a gene encoding a XET-related protein. YJ8 shows GUS-expression in 3–4 cells of the valve margin inner epidermis and at the sepal and petal abscission zones, and appears to be positively regulated by SHP1/2 (Østergaard et al., 2001).
Many other enzymatic activities are probably required to achieve pod shatter, such as those related to lignin synthesis, and others that still need to be proved to be related to dehiscence. With the completion of the Arabidopsis genome sequence and the comprehensive analysis of expression patterns and metabolic pathways currently underway, it is likely that a wealth of information will arise soon. It will be interesting to learn which other activities are needed and how to integrate this knowledge to get deeper insights into the physiology of dehiscence.
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Signalling and co-ordination |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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By contrast to the increasing number of transcription factors that have been related to DZ specification, little is known about the signalling mechanisms that must exist to ensure the co-ordination of events leading to pod shatter. The identification and characterization of regulatory elements in the promoters of the genes encoding the dehiscence-related enzymes listed above, and of putative targets of post-translational regulation in the encoded proteins could provide some insights as to how the process is co-ordinated. Such enzymatic activities are probably downstream in the regulatory cascade that originates with the transcription factors involved in DZ formation, but there are no consistent data on the nature and components of this cascade. So far, neither mechanisms of cell-to-cell communication nor signalling molecules have been identified as unequivocally related to this process. However, some candidates could be proposed based on diverse evidence.
Two putative membrane-bound proteins identified by the enhancer trap strategy could be suggested as participants based on sequence similarity and expression pattern analyses, although no functional data are reported yet. YJ80 shows reporter expression at the valve margin and in the seed abscission zone. The YJ80 T-DNA is inserted close to a gene encoding a protein with weak similarity to mammalian ankyrins, and which appears to be genetically downstream of SHP1/SHP2 and IND1 (Østergaard et al., 2001). The YJ115 T-DNA insertion is upstream of a gene of unknown function that contains a putative transmembrane domain. YJ115 shows reporter expression in the abaxial replum and the valve margins, and is regulated by the SHP genes (Roeder et al., 2001).
It has recently been reported that DEFENSE, NO DEATH1 (DND1), a gene encoding a cyclic nucleotide-gated ion channel (CNGC), is expressed in senescing organs and in the DZ of Arabidopsis siliques (Köhler et al., 2001). The dnd1 mutation was first recognized for producing a defective response to pathogen infection. dnd1 mutants are dwarf and, upon infection by avirulent pathogens, are unable to undergo the characteristic programmed cell death associated with the hypersensitive response (Yu et al., 1998). The CNGC encoded by DND1 is a membrane-protein able to conduct K+ and Ca2+ ions, a shared functional characteristic with other animal CNGCs involved in signal transduction (Leng et al., 1999). Although possible defects in dehiscence have not been studied in these mutants, it is tempting to speculate that the process of cell separation in the DZ could be affected by a failure in inducing specific programmed cell death.
As pointed out before, dehiscence and abscission are related processes. A leucine-rich repeat receptor-like protein kinase (LRR-RLK), HAESA, was shown to be involved in the regulation of floral organ abscission in Arabidopsis (Jinn et al., 2000). LRR-RKs are a large family in Arabidopsis, and some of their members have been related to different developmental processes based mainly on mutant phenotypes. Whether there is any LRR-RLK involved in fruit dehiscence regulation is still unknown, although it would be interesting to explore this possibility. SAC29 is an mRNA specifically up-regulated in Brassica napus DZ during late pod development. SAC29 encodes a protein with homology to the receiver domain of response regulator proteins (Whitelaw et al., 1999). In plants, several of these systems, organized in diverse modular arrangements, have been implicated in the response to different stimuli such as ethylene or cytokinin signals (reviewed in (D’Agostino and Kieber, 1999). Although no functional role has been assigned to SAC29, it represents an exciting starting point to study signal transduction mechanisms related to dehiscence.
Clearly, much work needs to be done to begin to clarify how fruit dehiscence is co-ordinated and which are the signals and signalling cascades involved. The study of the functional significance of some of the data presented above should be complemented with new efforts in this direction.
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Is there hormonal control of dehiscence? |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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Abscission processes have been linked by considerable evidence to the opposing action of the plant hormones ethylene and auxin (reviewed in González-Carranza et al., 1998). Ethylene works by promoting abscission, while auxins act to delay it. Together, the balance between these two hormones appears to be an important factor regulating the timing of abscission. The hormonal induction of pod dehiscence is less well characterized, although some studies have been reported suggesting similar responses. In studies on fruit development of Brassica parthenocarpic pods, a slightly delayed shattering was correlated with a reduced ethylene production, and normal timing of cell separation could be restored by the application of exogenous ethylene (Child et al., 1998). However, Arabidopsis mutants with non-functional ethylene receptors exhibit a normal time-course of silique dehiscence, suggesting that ethylene might have a minor role in shatter induction.
By contrast, auxins are likely to play a dominant role in dehiscence regulation. In Brassica, an increase in cellulase activity in the DZ was shown to correlate with a specific decrease in auxin content in those cells. In addition, the exogenous application of auxin analogues to Brassica developing pods significantly delayed, although it did not prevent, DZ cell separation (Chauvaux et al., 1997). It was observed that these auxin analogues inhibited the increase in cellulase activity and, interestingly, also affected RDPG1 pectinase activity by blocking its secretion into the cell wall (see above, Dal Degan et al., 2001).
Related to the possible role of auxin in dehiscence regulation the pattern of expression reported for the bHLH transcription factor SPATULA (SPT) is suggestive. In spt mutants the formation of the gynoecium apical tissues and the septum is reduced and the fertility is low. SPT is required for the development of carpel tissues specialized in pollen tube growth: stigma, style and transmitting tract (Alvarez and Smyth, 1999). However, SPT is not only expressed in the pollen tract tissues, but it shows a complex pattern of expression in many different tissues and developmental stages, indicating that SPT may act redundantly with other factors to control tissue growth. Especially intriguing is SPT expression related to cell separation: SPT mRNA is found in the anther stomiun, the DZ of grown siliques, and in the seed abscission zone (Heisler et al., 2001). Diverse evidence indicates that SPT is responsive to auxin: it has been shown that ETTIN, an Auxin Response Factor (ARF), represses SPT in some carpel tissues (Sessions et al., 1997; Heisler et al., 2001); several Auxin Response Elements, the binding motifs for ARFs, are found in the SPT promoter, and it appears that, together with repression by ETT, other ARFs could activate SPT expression (Heisler et al., 2001); finally, inhibitors of auxin polar transport suppress spt carpel phenotypes (Nemhauser et al., 2000). It would be interesting to explore whether SPT could be a link between cell differentiation and auxin action related to DZ formation, and other separation processes such as anther dehiscence or seed abscission.
Pod dehiscence and seed abscission are likely to be co-ordinated, and they could share common regulatory signals. Meakin and Roberts (1991) confirmed this correlation in infection-induced pod dehiscence of Brassica fruits. In addition, some of the genes described above, including RDPG1, YJ80-reported gene, and SPT, are expressed in both dehiscence and seed abscission zones and a functional relationship has been established between DZ genes (SHP, Pinyopich et al., 2001). What could be those common signals? So far, little evidence exists to propose such a mechanism, but abscisic acid may be suggested as a possible co-ordinating signal: its role in seed development is well established, and it has been related to the regulation of programmed cell death in processes like cereal seed germination (Young and Gallie, 2000). A parallel can be proposed between pod shatter and anther dehiscence. These are analogous processes of cell separation that share a number of specifically expressed genes (RDPG1, SPT, see above). Jasmonic acid (JA) has been related to anther dehiscence, and mutants defective in JA synthesis show an altered timing of anther opening (Ishiguro et al., 2001; Sanders et al., 2000). So far, there are no reports of a possible role for JA in pod shattering, but the search for a common signalling factor between anther and pod dehiscence is still far from extensive.
It appears that hormone action could have a role in both DZ differentiation and the co-ordination of physiological events leading to cell separation. Few studies have directly addressed these questions so far, but a large collection of Arabidopsis mutants affected in different hormone synthetic pathways or hormone responses is available that could be used for further characterization of the role of these likely regulators.
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Summary |
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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The study of dehiscence regulation has important biotechnological potential and could be of great applicability in manipulating seed dispersal in many crops. DZ formation also provides a great system to study tissue specification from a basic science point of view. From these studies, it appears that regulation of cell differentiation involves many factors that interact in a complex network (Fig. 2). The characterization of novel genes acting at this level and the analyses of the regulatory interactions among all of them could be the key to understanding how the different cell fates are established and the physiological events co-ordinated both spatially and temporally. The identification of the signalling cascade(s) involved in co-ordinating the process is still a major issue and much work needs to be done in this direction, but there are already some indications of the paths that should be explored. Solving the many questions posed is an attractive challenge already undertaken by several researchers, and could open the door to new insights in cell differentiation issues, not only those directly related to dehiscence, but also with a broader perspective.
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Acknowledgements |
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I would like to thank Soraya Pelaz, Antonio Martínez-Laborda and Francisco Madueño for critical reading of the manuscript, and Barbara Ambrose and Adrienne Roeder for correcting style and grammar. I would also like to thank Marty Yanofsky and members of his laboratory for stimulating discussion on the subject. This work is supported by the Spanish Ministerio de Ciencia y Tecnología.
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TopAbstractIntroductionThe dehiscence processThe genetics of pod...The regulation of DZ...The downstream effectorsSignalling and co-ordinationIs there hormonal control...SummaryReferences |
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