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Interactions of CUP-SHAPED COTYLEDON and SPATULA genes control carpel margin development in Arabidopsis thaliana.

Nahar MA, Ishida T, Smyth DR, Tasaka M, Aida M - Plant Cell Physiol. (2012)

Bottom Line: In spt, transcripts of both CUC genes accumulated ectopically, and addition of cuc1 and cuc2 mutations to spt suppressed the split phenotype of carpels specifically along their lateral margins.In the basal gynoecium, on the other hand, all three genes promoted the formation of margin-derived structures, as revealed by the synergistic interactions of spt with each of the cuc mutations.Our results suggest that differential interactions among SPT, CUC1 and CUC2 direct the formation of domain-specific structures of the Arabidopsis gynoecium.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara, 630-0192 Japan.

ABSTRACT
A characteristic feature of flowering plants is the fusion of carpels, which results in the formation of an enclosed gynoecium. In Arabidopsis thaliana, the gynoecium is formed by the fusion of two carpels along their margins, which also act as a meristematic site for the formation of internal structures such as ovules, the septum and transmitting tract. How gene interactions coordinate the fusion and differentiation of the marginal structures during gynoecium development is largely unknown. It was previously shown that the SPATULA (SPT) gene is required for carpel fusion, whereas overexpression of the CUP-SHAPED COTYLEDON genes CUC1 and CUC2 prevents it. Here we provide evidence that SPT promotes carpel fusion in the apical gynoecium partly through the negative regulation of CUC1 and CUC2 expression. In spt, transcripts of both CUC genes accumulated ectopically, and addition of cuc1 and cuc2 mutations to spt suppressed the split phenotype of carpels specifically along their lateral margins. In the basal gynoecium, on the other hand, all three genes promoted the formation of margin-derived structures, as revealed by the synergistic interactions of spt with each of the cuc mutations. Our results suggest that differential interactions among SPT, CUC1 and CUC2 direct the formation of domain-specific structures of the Arabidopsis gynoecium.

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A model for the control of apical carpel fusion by SPT, CUC1 and CUC2 in the Arabidopsis gynoecium. The closure of the apical gynoecium in the region of the style and stigma results from the combination of two types of growth activities: upward growth of the gynoecial tube ensures congenital fusion of carpels along their lateral margins (dashed red line), and inward growth of the medial ridges fills up the central hollow of the style and closes the top. SPT represses CUC1 and CUC2 expression to ensure the upward growth (orange arrows). Inward growth (green arrows) of the apical medial ridges is promoted by SPT but does not involve CUC1 and CUC2 activities.
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pcs057-F7: A model for the control of apical carpel fusion by SPT, CUC1 and CUC2 in the Arabidopsis gynoecium. The closure of the apical gynoecium in the region of the style and stigma results from the combination of two types of growth activities: upward growth of the gynoecial tube ensures congenital fusion of carpels along their lateral margins (dashed red line), and inward growth of the medial ridges fills up the central hollow of the style and closes the top. SPT represses CUC1 and CUC2 expression to ensure the upward growth (orange arrows). Inward growth (green arrows) of the apical medial ridges is promoted by SPT but does not involve CUC1 and CUC2 activities.

Mentions: The suppression of the spt phenotype by cuc1 and cuc2 indicates that the defect of spt in congenital fusion is dependent on the activities of CUC1 and CUC2, and our expression data are consistent with this notion. In the wild-type apical region, SPT expression is detected throughout the medial domain (Heisler et al. 2001; Fig. 6A). In the same domain, CUC1 is not expressed and CUC2 expression is restricted to the adaxial domain. In spt, on the other hand, both of these genes are ectopically expressed throughout the medial domain. Taken together, these results indicate that SPT negatively regulates the expression of CUC1 and CUC2 in the apical region of the gynoecial primordium, and that this repression is essential for complete congenital fusion of the carpels along their lateral margins (Fig. 7, orange arrows). On the other hand, no detectable contribution of CUC1 and CUC2 to the medial ridge growth and subsequent post-genital fusion in the centrally apical gynoecium of spt was found, indicating that only SPT is involved in post-genital fusion to form a solid style (Fig. 7, green arrows).Fig. 7


Interactions of CUP-SHAPED COTYLEDON and SPATULA genes control carpel margin development in Arabidopsis thaliana.

Nahar MA, Ishida T, Smyth DR, Tasaka M, Aida M - Plant Cell Physiol. (2012)

A model for the control of apical carpel fusion by SPT, CUC1 and CUC2 in the Arabidopsis gynoecium. The closure of the apical gynoecium in the region of the style and stigma results from the combination of two types of growth activities: upward growth of the gynoecial tube ensures congenital fusion of carpels along their lateral margins (dashed red line), and inward growth of the medial ridges fills up the central hollow of the style and closes the top. SPT represses CUC1 and CUC2 expression to ensure the upward growth (orange arrows). Inward growth (green arrows) of the apical medial ridges is promoted by SPT but does not involve CUC1 and CUC2 activities.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3367164&req=5

pcs057-F7: A model for the control of apical carpel fusion by SPT, CUC1 and CUC2 in the Arabidopsis gynoecium. The closure of the apical gynoecium in the region of the style and stigma results from the combination of two types of growth activities: upward growth of the gynoecial tube ensures congenital fusion of carpels along their lateral margins (dashed red line), and inward growth of the medial ridges fills up the central hollow of the style and closes the top. SPT represses CUC1 and CUC2 expression to ensure the upward growth (orange arrows). Inward growth (green arrows) of the apical medial ridges is promoted by SPT but does not involve CUC1 and CUC2 activities.
Mentions: The suppression of the spt phenotype by cuc1 and cuc2 indicates that the defect of spt in congenital fusion is dependent on the activities of CUC1 and CUC2, and our expression data are consistent with this notion. In the wild-type apical region, SPT expression is detected throughout the medial domain (Heisler et al. 2001; Fig. 6A). In the same domain, CUC1 is not expressed and CUC2 expression is restricted to the adaxial domain. In spt, on the other hand, both of these genes are ectopically expressed throughout the medial domain. Taken together, these results indicate that SPT negatively regulates the expression of CUC1 and CUC2 in the apical region of the gynoecial primordium, and that this repression is essential for complete congenital fusion of the carpels along their lateral margins (Fig. 7, orange arrows). On the other hand, no detectable contribution of CUC1 and CUC2 to the medial ridge growth and subsequent post-genital fusion in the centrally apical gynoecium of spt was found, indicating that only SPT is involved in post-genital fusion to form a solid style (Fig. 7, green arrows).Fig. 7

Bottom Line: In spt, transcripts of both CUC genes accumulated ectopically, and addition of cuc1 and cuc2 mutations to spt suppressed the split phenotype of carpels specifically along their lateral margins.In the basal gynoecium, on the other hand, all three genes promoted the formation of margin-derived structures, as revealed by the synergistic interactions of spt with each of the cuc mutations.Our results suggest that differential interactions among SPT, CUC1 and CUC2 direct the formation of domain-specific structures of the Arabidopsis gynoecium.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara, 630-0192 Japan.

ABSTRACT
A characteristic feature of flowering plants is the fusion of carpels, which results in the formation of an enclosed gynoecium. In Arabidopsis thaliana, the gynoecium is formed by the fusion of two carpels along their margins, which also act as a meristematic site for the formation of internal structures such as ovules, the septum and transmitting tract. How gene interactions coordinate the fusion and differentiation of the marginal structures during gynoecium development is largely unknown. It was previously shown that the SPATULA (SPT) gene is required for carpel fusion, whereas overexpression of the CUP-SHAPED COTYLEDON genes CUC1 and CUC2 prevents it. Here we provide evidence that SPT promotes carpel fusion in the apical gynoecium partly through the negative regulation of CUC1 and CUC2 expression. In spt, transcripts of both CUC genes accumulated ectopically, and addition of cuc1 and cuc2 mutations to spt suppressed the split phenotype of carpels specifically along their lateral margins. In the basal gynoecium, on the other hand, all three genes promoted the formation of margin-derived structures, as revealed by the synergistic interactions of spt with each of the cuc mutations. Our results suggest that differential interactions among SPT, CUC1 and CUC2 direct the formation of domain-specific structures of the Arabidopsis gynoecium.

Show MeSH
Related in: MedlinePlus