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The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants.

Colasanti J, Tremblay R, Wong AY, Coneva V, Kozaki A, Mable BK - BMC Genomics (2006)

Bottom Line: The maize INDETERMINATE1 gene, ID1, is a key regulator of the transition to flowering and the founding member of a transcription factor gene family that encodes a protein with a distinct arrangement of zinc finger motifs.The zinc fingers and surrounding sequence make up the signature ID domain (IDD), which appears to be found in all higher plant genomes.These similarities between ID1 and closely related genes in other grasses point to possible similarities in function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada. jcolasan@uoguelph.ca

ABSTRACT

Background: The maize INDETERMINATE1 gene, ID1, is a key regulator of the transition to flowering and the founding member of a transcription factor gene family that encodes a protein with a distinct arrangement of zinc finger motifs. The zinc fingers and surrounding sequence make up the signature ID domain (IDD), which appears to be found in all higher plant genomes. The presence of zinc finger domains and previous biochemical studies showing that ID1 binds to DNA suggests that members of this gene family are involved in transcriptional regulation.

Results: Comparison of IDD genes identified in Arabidopsis and rice genomes, and all IDD genes discovered in maize EST and genomic databases, suggest that ID1 is a unique member of this gene family. High levels of sequence similarity amongst all IDD genes from maize, rice and Arabidopsis suggest that they are derived from a common ancestor. Several unique features of ID1 suggest that it is a divergent member of the maize IDD family. Although no clear ID1 ortholog was identified in the Arabidopsis genome, highly similar genes that encode proteins with identity extending beyond the ID domain were isolated from rice and sorghum. Phylogenetic comparisons show that these putative orthologs, along with maize ID1, form a group separate from other IDD genes. In contrast to ID1 mRNA, which is detected exclusively in immature leaves, several maize IDD genes showed a broad range of expression in various tissues. Further, Western analysis with an antibody that cross-reacts with ID1 protein and potential orthologs from rice and sorghum shows that all three proteins are detected in immature leaves only.

Conclusion: Comparative genomic analysis shows that the IDD zinc finger family is highly conserved among both monocots and dicots. The leaf-specific ID1 expression pattern distinguishes it from other maize IDD genes examined. A similar leaf-specific localization pattern was observed for the putative ID1 protein orthologs from rice and sorghum. These similarities between ID1 and closely related genes in other grasses point to possible similarities in function.

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Northern blot showing expression of 7 maize IDD genes compared to ID1. Gene-specific probes are indicated on the right side. Tissues used include: S, stem below the apical region, Ap, apical region of plant, including 2 cm above apical meristem and leaf primordia. Sections 1, 2 and 3 are immature leaf sections from 2–4 cm, 4–6 cm and 6–8 cm above the apex, respectively. TL, immature flag leaf surrounding tassel primordium; T, pre-anthesis tassel; R, roots. The same B73 plant with 7 visible leaves was used for sections S, Ap, 1, 2 and 3. (A) Gene-specific probes derived from cDNAs of ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9. The ZmCDC2 probe, which is detected in tissues with actively dividing cells, was used as a control [38]. An arrowhead indicates the position of the ZmIDDp10 band. (B) Blot hybridized with specific probes to ZmIDD3, ZmIDD7, ZmIDD13 and an actin-specific probe.
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Figure 4: Northern blot showing expression of 7 maize IDD genes compared to ID1. Gene-specific probes are indicated on the right side. Tissues used include: S, stem below the apical region, Ap, apical region of plant, including 2 cm above apical meristem and leaf primordia. Sections 1, 2 and 3 are immature leaf sections from 2–4 cm, 4–6 cm and 6–8 cm above the apex, respectively. TL, immature flag leaf surrounding tassel primordium; T, pre-anthesis tassel; R, roots. The same B73 plant with 7 visible leaves was used for sections S, Ap, 1, 2 and 3. (A) Gene-specific probes derived from cDNAs of ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9. The ZmCDC2 probe, which is detected in tissues with actively dividing cells, was used as a control [38]. An arrowhead indicates the position of the ZmIDDp10 band. (B) Blot hybridized with specific probes to ZmIDD3, ZmIDD7, ZmIDD13 and an actin-specific probe.

Mentions: A previous study found that ID1 mRNA is expressed only in immature leaves and is not detectable in the shoot apical meristem region, leaf primordia or in mature leaves [22]. This highly specific expression pattern suggests that ID1 has a role in mediating the production or the transmission of a leaf-derived floral inductive signal [10]. To compare the ID1 expression pattern with other maize IDD genes we used Northern hybridization and gene-specific probes to the 4 IDD genes isolated from maize cDNA libraries: ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9, as well as 3 other ZmIDD genes, ZmIDD3, ZmIDD7, ZmIDD13, with probes isolated by PCR (Figure 4). We found that each of these 7 maize IDD genes had distinct expression patterns and that none of them exhibited tissue-specific expression similar to ID1 (Figure 4). In all cases the range of expression is broader than ID1, with mRNA of ZmIDD genes detected in most plant tissues (Figure 4). For example, whereas ID1 mRNA is confined to immature leaves and is clearly absent from other shoot tissues, ZmIDDp1 mRNA is detected in all vegetative tissues, and is especially abundant in tissues enriched for shoot and root apical meristems (Figure 4A). Similar to ID1, the ZmIDDp10 gene is detected in immature leaves, albeit at a much lower level, but it is also expressed at low levels in root and is barely detectable in floral tissues (Figure 4A). ZmIDDveg9, which was isolated from a vegetative shoot apex cDNA library, is detected in apical meristem-enriched tissues, but is also found in immature leaves, roots and, at a lesser level, in tassels (Figure 4A). In contrast, ZmIDDveg7, which was isolated from the same vegetative meristem cDNA library as ZmIDDveg9, shows a similar expression pattern, except that it is expressed at higher levels in floral tissues and it is detected in apical regions and leaf primordia but to a lesser extent in more developed immature leaves.


The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants.

Colasanti J, Tremblay R, Wong AY, Coneva V, Kozaki A, Mable BK - BMC Genomics (2006)

Northern blot showing expression of 7 maize IDD genes compared to ID1. Gene-specific probes are indicated on the right side. Tissues used include: S, stem below the apical region, Ap, apical region of plant, including 2 cm above apical meristem and leaf primordia. Sections 1, 2 and 3 are immature leaf sections from 2–4 cm, 4–6 cm and 6–8 cm above the apex, respectively. TL, immature flag leaf surrounding tassel primordium; T, pre-anthesis tassel; R, roots. The same B73 plant with 7 visible leaves was used for sections S, Ap, 1, 2 and 3. (A) Gene-specific probes derived from cDNAs of ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9. The ZmCDC2 probe, which is detected in tissues with actively dividing cells, was used as a control [38]. An arrowhead indicates the position of the ZmIDDp10 band. (B) Blot hybridized with specific probes to ZmIDD3, ZmIDD7, ZmIDD13 and an actin-specific probe.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 4: Northern blot showing expression of 7 maize IDD genes compared to ID1. Gene-specific probes are indicated on the right side. Tissues used include: S, stem below the apical region, Ap, apical region of plant, including 2 cm above apical meristem and leaf primordia. Sections 1, 2 and 3 are immature leaf sections from 2–4 cm, 4–6 cm and 6–8 cm above the apex, respectively. TL, immature flag leaf surrounding tassel primordium; T, pre-anthesis tassel; R, roots. The same B73 plant with 7 visible leaves was used for sections S, Ap, 1, 2 and 3. (A) Gene-specific probes derived from cDNAs of ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9. The ZmCDC2 probe, which is detected in tissues with actively dividing cells, was used as a control [38]. An arrowhead indicates the position of the ZmIDDp10 band. (B) Blot hybridized with specific probes to ZmIDD3, ZmIDD7, ZmIDD13 and an actin-specific probe.
Mentions: A previous study found that ID1 mRNA is expressed only in immature leaves and is not detectable in the shoot apical meristem region, leaf primordia or in mature leaves [22]. This highly specific expression pattern suggests that ID1 has a role in mediating the production or the transmission of a leaf-derived floral inductive signal [10]. To compare the ID1 expression pattern with other maize IDD genes we used Northern hybridization and gene-specific probes to the 4 IDD genes isolated from maize cDNA libraries: ZmIDDp1, ZmIDDp10, ZmIDDveg7 and ZmIDDveg9, as well as 3 other ZmIDD genes, ZmIDD3, ZmIDD7, ZmIDD13, with probes isolated by PCR (Figure 4). We found that each of these 7 maize IDD genes had distinct expression patterns and that none of them exhibited tissue-specific expression similar to ID1 (Figure 4). In all cases the range of expression is broader than ID1, with mRNA of ZmIDD genes detected in most plant tissues (Figure 4). For example, whereas ID1 mRNA is confined to immature leaves and is clearly absent from other shoot tissues, ZmIDDp1 mRNA is detected in all vegetative tissues, and is especially abundant in tissues enriched for shoot and root apical meristems (Figure 4A). Similar to ID1, the ZmIDDp10 gene is detected in immature leaves, albeit at a much lower level, but it is also expressed at low levels in root and is barely detectable in floral tissues (Figure 4A). ZmIDDveg9, which was isolated from a vegetative shoot apex cDNA library, is detected in apical meristem-enriched tissues, but is also found in immature leaves, roots and, at a lesser level, in tassels (Figure 4A). In contrast, ZmIDDveg7, which was isolated from the same vegetative meristem cDNA library as ZmIDDveg9, shows a similar expression pattern, except that it is expressed at higher levels in floral tissues and it is detected in apical regions and leaf primordia but to a lesser extent in more developed immature leaves.

Bottom Line: The maize INDETERMINATE1 gene, ID1, is a key regulator of the transition to flowering and the founding member of a transcription factor gene family that encodes a protein with a distinct arrangement of zinc finger motifs.The zinc fingers and surrounding sequence make up the signature ID domain (IDD), which appears to be found in all higher plant genomes.These similarities between ID1 and closely related genes in other grasses point to possible similarities in function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada. jcolasan@uoguelph.ca

ABSTRACT

Background: The maize INDETERMINATE1 gene, ID1, is a key regulator of the transition to flowering and the founding member of a transcription factor gene family that encodes a protein with a distinct arrangement of zinc finger motifs. The zinc fingers and surrounding sequence make up the signature ID domain (IDD), which appears to be found in all higher plant genomes. The presence of zinc finger domains and previous biochemical studies showing that ID1 binds to DNA suggests that members of this gene family are involved in transcriptional regulation.

Results: Comparison of IDD genes identified in Arabidopsis and rice genomes, and all IDD genes discovered in maize EST and genomic databases, suggest that ID1 is a unique member of this gene family. High levels of sequence similarity amongst all IDD genes from maize, rice and Arabidopsis suggest that they are derived from a common ancestor. Several unique features of ID1 suggest that it is a divergent member of the maize IDD family. Although no clear ID1 ortholog was identified in the Arabidopsis genome, highly similar genes that encode proteins with identity extending beyond the ID domain were isolated from rice and sorghum. Phylogenetic comparisons show that these putative orthologs, along with maize ID1, form a group separate from other IDD genes. In contrast to ID1 mRNA, which is detected exclusively in immature leaves, several maize IDD genes showed a broad range of expression in various tissues. Further, Western analysis with an antibody that cross-reacts with ID1 protein and potential orthologs from rice and sorghum shows that all three proteins are detected in immature leaves only.

Conclusion: Comparative genomic analysis shows that the IDD zinc finger family is highly conserved among both monocots and dicots. The leaf-specific ID1 expression pattern distinguishes it from other maize IDD genes examined. A similar leaf-specific localization pattern was observed for the putative ID1 protein orthologs from rice and sorghum. These similarities between ID1 and closely related genes in other grasses point to possible similarities in function.

Show MeSH