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Genome-wide characterization, expression and functional analysis of CLV3/ESR gene family in tomato.

Zhang Y, Yang S, Song Y, Wang J - BMC Genomics (2014)

Bottom Line: In particular, SlCLE12, the homologue of Arabidopsis CLE41/44 gene, appears to be the dominant CLE gene in most of tested tissues with its maximum expression found in vascular tissues.Upon the treatment with synthetic peptides corresponding to the 12-aa CLE domains of SlCLE 10, 12 and 13, tomato seedlings exhibit a clear reduction in root length to varying degrees.Differential expression patterns of various SlCLEs provide important insights into the functional divergence of CLE signaling cascade in Solanaceae species, especially their potential involvements in the regulation of fruit development and ripening.

View Article: PubMed Central - PubMed

Affiliation: School of Environmental Science and Engineering, Tianjin University, Weijin Rd, 92#, Nankai District, Tianjin 300072, China. jiehuawang@tju.edu.cn.

ABSTRACT

Background: By encoding a group of small secretory peptides, the members of the CLAVATA3/EMBRYO-SURROUNDING REGION (CLE) family play important roles in cell-to-cell communication to control the balance between stem cell proliferation and differentiation in plant development. Despite recent identification and characterization of members of this gene family in several plant species, little is known about its functional role in plants with fleshy fruits.

Results: In total, fifteen CLE genes (SlCLE1-15) were identified from tomato (Solanum lycopersicum cv. 'Heinz-1706') genome and their multiple characters including phylogeny, gene structures, chromosome locations, conserved motifs and cis-elements in the promoter sequences, were analyzed. Real-time PCR analysis showed that 13 out of 15 identified SlCLE genes are transcribed and exhibit remarkably unique expression patterns among tissues and organs. In particular, SlCLE12, the homologue of Arabidopsis CLE41/44 gene, appears to be the dominant CLE gene in most of tested tissues with its maximum expression found in vascular tissues. Meanwhile, SlCLE1, 10, 13 exhibit specific but distinct expression in flower bud, root and shoot apex, respectively. More notably, several SlCLEs are dramatically regulated in their transcriptional levels during fruit development and ripening, indicating significant role these genes may potentially play in the critical physiological process. Upon the treatment with synthetic peptides corresponding to the 12-aa CLE domains of SlCLE 10, 12 and 13, tomato seedlings exhibit a clear reduction in root length to varying degrees.

Conclusions: This study provides a comprehensive genomic analysis of CLE gene family in tomato, a crop species with fleshy fruit. Differential expression patterns of various SlCLEs provide important insights into the functional divergence of CLE signaling cascade in Solanaceae species, especially their potential involvements in the regulation of fruit development and ripening.

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Phenotypes of 10-d tomato seedlings upon the treatment of SlCLE motif peptides. (A) Effect of 100 μM concentration of SlCLE10p, 12p and 13p on 10-day old tomato seedling development. (B) Effects of different SlCLE motif peptides on the root length of tomato seedlings. The lengths of the main roots were measured after 10 d of growth on peptide-containing media (n = 25 for each treatment). Data and error bars represent mean ± SD.
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Fig4: Phenotypes of 10-d tomato seedlings upon the treatment of SlCLE motif peptides. (A) Effect of 100 μM concentration of SlCLE10p, 12p and 13p on 10-day old tomato seedling development. (B) Effects of different SlCLE motif peptides on the root length of tomato seedlings. The lengths of the main roots were measured after 10 d of growth on peptide-containing media (n = 25 for each treatment). Data and error bars represent mean ± SD.

Mentions: In Arabidopsis, the specificity of CLE function has been proposed to be mainly achieved by differential expression patterns of CLE genes. In order to gain insights into the potential biological roles of SlCLEs, we analyzed their temporal and spatial expression profiles in various tissues and fruits at different developmental stages using qRT-PCR (Additional file7 and Figure 3). In Arabidopsis, all but one of the 32 AtCLE genes are transcribed[33]. In tomato, thirteen out of fifteen SlCLEs were able to be cloned from a pooled cDNA derived from an array of tomato tissues. All tissues examined express multiple SlCLE genes and the overlap among different CLE gene expression patterns was conspicuous (Additional file7 and Figure 3). In brief, the expression level of all SlCLEs is low in small green fruit and increases after the breaker stage (Additional file6 and Figure 4). SlCLE2, 3, 4, 6, 7, and 14 exhibit a relatively uniform expression among the examined tissues; however, the remaining SlCLEs exhibit a quite differential expression pattern among tissues and organs (Additional file7 and Figure 3). Notably, SlCLE12 appears to be the most abundantly expressed SlCLE in almost all tested tissues except for the green fruit of 1 cm size (Additional file7 and Figure 3). In Arabidopsis, an exactly same CLE peptide (TDIF) as SlCLE12p and a very similar one are produced by CLE41/44 and CLE42, respectively[2, 40]. Using the GUS (β-glucuronidase) reporter gene assay, CLE41/44 are found to be expressed preferentially in vascular bundles, while CLE42 is expressed strongly in SAM and axillary meristems. Therefore, CLE41/44 and CLE42 have been suggested to play roles in regulating wood development[41–43] and the meristematic activity[44], respectively. Considering its vascular-specific expression, SlCLE12 could be most likely denoted as the orthologue of CLE41/44 in tomato; however, its broad and significant expression in a range of tissues and organs imply an even higher functional diversity or a basic function of TDIF in regulating biological processes. As an evidence, a novel function in enhancing axillary bud formation has been recently disclosed for Arabidopsis TDIF peptide[44].Figure 3


Genome-wide characterization, expression and functional analysis of CLV3/ESR gene family in tomato.

Zhang Y, Yang S, Song Y, Wang J - BMC Genomics (2014)

Phenotypes of 10-d tomato seedlings upon the treatment of SlCLE motif peptides. (A) Effect of 100 μM concentration of SlCLE10p, 12p and 13p on 10-day old tomato seedling development. (B) Effects of different SlCLE motif peptides on the root length of tomato seedlings. The lengths of the main roots were measured after 10 d of growth on peptide-containing media (n = 25 for each treatment). Data and error bars represent mean ± SD.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4195864&req=5

Fig4: Phenotypes of 10-d tomato seedlings upon the treatment of SlCLE motif peptides. (A) Effect of 100 μM concentration of SlCLE10p, 12p and 13p on 10-day old tomato seedling development. (B) Effects of different SlCLE motif peptides on the root length of tomato seedlings. The lengths of the main roots were measured after 10 d of growth on peptide-containing media (n = 25 for each treatment). Data and error bars represent mean ± SD.
Mentions: In Arabidopsis, the specificity of CLE function has been proposed to be mainly achieved by differential expression patterns of CLE genes. In order to gain insights into the potential biological roles of SlCLEs, we analyzed their temporal and spatial expression profiles in various tissues and fruits at different developmental stages using qRT-PCR (Additional file7 and Figure 3). In Arabidopsis, all but one of the 32 AtCLE genes are transcribed[33]. In tomato, thirteen out of fifteen SlCLEs were able to be cloned from a pooled cDNA derived from an array of tomato tissues. All tissues examined express multiple SlCLE genes and the overlap among different CLE gene expression patterns was conspicuous (Additional file7 and Figure 3). In brief, the expression level of all SlCLEs is low in small green fruit and increases after the breaker stage (Additional file6 and Figure 4). SlCLE2, 3, 4, 6, 7, and 14 exhibit a relatively uniform expression among the examined tissues; however, the remaining SlCLEs exhibit a quite differential expression pattern among tissues and organs (Additional file7 and Figure 3). Notably, SlCLE12 appears to be the most abundantly expressed SlCLE in almost all tested tissues except for the green fruit of 1 cm size (Additional file7 and Figure 3). In Arabidopsis, an exactly same CLE peptide (TDIF) as SlCLE12p and a very similar one are produced by CLE41/44 and CLE42, respectively[2, 40]. Using the GUS (β-glucuronidase) reporter gene assay, CLE41/44 are found to be expressed preferentially in vascular bundles, while CLE42 is expressed strongly in SAM and axillary meristems. Therefore, CLE41/44 and CLE42 have been suggested to play roles in regulating wood development[41–43] and the meristematic activity[44], respectively. Considering its vascular-specific expression, SlCLE12 could be most likely denoted as the orthologue of CLE41/44 in tomato; however, its broad and significant expression in a range of tissues and organs imply an even higher functional diversity or a basic function of TDIF in regulating biological processes. As an evidence, a novel function in enhancing axillary bud formation has been recently disclosed for Arabidopsis TDIF peptide[44].Figure 3

Bottom Line: In particular, SlCLE12, the homologue of Arabidopsis CLE41/44 gene, appears to be the dominant CLE gene in most of tested tissues with its maximum expression found in vascular tissues.Upon the treatment with synthetic peptides corresponding to the 12-aa CLE domains of SlCLE 10, 12 and 13, tomato seedlings exhibit a clear reduction in root length to varying degrees.Differential expression patterns of various SlCLEs provide important insights into the functional divergence of CLE signaling cascade in Solanaceae species, especially their potential involvements in the regulation of fruit development and ripening.

View Article: PubMed Central - PubMed

Affiliation: School of Environmental Science and Engineering, Tianjin University, Weijin Rd, 92#, Nankai District, Tianjin 300072, China. jiehuawang@tju.edu.cn.

ABSTRACT

Background: By encoding a group of small secretory peptides, the members of the CLAVATA3/EMBRYO-SURROUNDING REGION (CLE) family play important roles in cell-to-cell communication to control the balance between stem cell proliferation and differentiation in plant development. Despite recent identification and characterization of members of this gene family in several plant species, little is known about its functional role in plants with fleshy fruits.

Results: In total, fifteen CLE genes (SlCLE1-15) were identified from tomato (Solanum lycopersicum cv. 'Heinz-1706') genome and their multiple characters including phylogeny, gene structures, chromosome locations, conserved motifs and cis-elements in the promoter sequences, were analyzed. Real-time PCR analysis showed that 13 out of 15 identified SlCLE genes are transcribed and exhibit remarkably unique expression patterns among tissues and organs. In particular, SlCLE12, the homologue of Arabidopsis CLE41/44 gene, appears to be the dominant CLE gene in most of tested tissues with its maximum expression found in vascular tissues. Meanwhile, SlCLE1, 10, 13 exhibit specific but distinct expression in flower bud, root and shoot apex, respectively. More notably, several SlCLEs are dramatically regulated in their transcriptional levels during fruit development and ripening, indicating significant role these genes may potentially play in the critical physiological process. Upon the treatment with synthetic peptides corresponding to the 12-aa CLE domains of SlCLE 10, 12 and 13, tomato seedlings exhibit a clear reduction in root length to varying degrees.

Conclusions: This study provides a comprehensive genomic analysis of CLE gene family in tomato, a crop species with fleshy fruit. Differential expression patterns of various SlCLEs provide important insights into the functional divergence of CLE signaling cascade in Solanaceae species, especially their potential involvements in the regulation of fruit development and ripening.

Show MeSH