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Identification and Expression Analysis of Ribosome Biogenesis Factor Co-orthologs in Solanum lycopersicum.

Simm S, Fragkostefanakis S, Paul P, Keller M, Einloft J, Scharf KD, Schleiff E - Bioinform Biol Insights (2015)

Bottom Line: In combination with existing expression profiles, we can conclude that co-orthologs of RBFs by large account for a preferential function in different tissue or at distinct developmental stages.In addition, co-regulated clusters of RBF and RP coding genes have been observed.The relevance of these results is discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, Frankfurt/Main, Germany. ; Cluster of Excellence Frankfurt, Goethe University, Frankfurt/Main, Germany.

ABSTRACT
Ribosome biogenesis involves a large inventory of proteinaceous and RNA cofactors. More than 250 ribosome biogenesis factors (RBFs) have been described in yeast. These factors are involved in multiple aspects like rRNA processing, folding, and modification as well as in ribosomal protein (RP) assembly. Considering the importance of RBFs for particular developmental processes, we examined the complexity of RBF and RP (co-)orthologs by bioinformatic assignment in 14 different plant species and expression profiling in the model crop Solanum lycopersicum. Assigning (co-)orthologs to each RBF revealed that at least 25% of all predicted RBFs are encoded by more than one gene. At first we realized that the occurrence of multiple RBF co-orthologs is not globally correlated to the existence of multiple RP co-orthologs. The transcript abundance of genes coding for predicted RBFs and RPs in leaves and anthers of S. lycopersicum was determined by next generation sequencing (NGS). In combination with existing expression profiles, we can conclude that co-orthologs of RBFs by large account for a preferential function in different tissue or at distinct developmental stages. This notion is supported by the differential expression of selected RBFs during male gametophyte development. In addition, co-regulated clusters of RBF and RP coding genes have been observed. The relevance of these results is discussed.

No MeSH data available.


The expression profile of RBF encoded by multiple genes. The expression values (Supplementary Table 4) for genes coding for RBFs with multiple co-orthologs have been normalized to the individual maximal value given next to the panel and the expression profile is shown (scale on the right). The order of samples is indicated on the right, legend in bold indicates the MACE results; the rest of the samples are derived from the NGS data.33Abbreviations: fmg: fruit mature green; fb: fruit breaker; fr: fruit ripe.
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f9-bbi-9-2015-001: The expression profile of RBF encoded by multiple genes. The expression values (Supplementary Table 4) for genes coding for RBFs with multiple co-orthologs have been normalized to the individual maximal value given next to the panel and the expression profile is shown (scale on the right). The order of samples is indicated on the right, legend in bold indicates the MACE results; the rest of the samples are derived from the NGS data.33Abbreviations: fmg: fruit mature green; fb: fruit breaker; fr: fruit ripe.

Mentions: In general, about 25% of all RBFs predicted in A. thaliana and tomato are encoded by at least two different genes, which applies for all complexes involved in ribosome biogenesis (Figs. 2–4). The genes coding for RBFs are more strongly expressed in anther compared to leaf (Fig. 6; Table 3), which is not surprising, considering that anther is a male reproductive organ undergoing rapid metabolic changes. However, we also observed genes that show a stronger expression in leaves. These are mostly RBFs represented by multiple co-orthologs (Table 3), which is a hint for a tissue-specific set of assembly factors for ribosome biogenesis. In-depth analysis of the expression pattern of tomato RBFs with multiple co-orthologs in different tissues revealed differential expression for all (Fig. 9). Thus, we can conclude that the co-orthologs to individual RBFs found in plants account for a preferential expression in distinct tissues or at different developmental stages. This is consistent with the observed variation of the number of RBFs to which co-orthologs could be assigned (Fig. 2B). We conclude that plant ribosome biogenesis requires the action of tissue- or developmental stage-specific factors, which is in agreement with reports showing tissue-specific developmental defects in some RBF mutants.16,17,19,39 On the other hand, considering the critical function of individual RBFs for a vital cellular process like ribosome biogenesis, we can assume that other proteins with similar functions might compensate for the factors not predicted in any plant, a hypothesis that needs to be experimentally challenged in the future. On the other hand, the absence of some factors in plants might be explained by differences in the processing pathway compared to yeast, since for example, not all cleavage sites on plant rRNA have been mapped so far.


Identification and Expression Analysis of Ribosome Biogenesis Factor Co-orthologs in Solanum lycopersicum.

Simm S, Fragkostefanakis S, Paul P, Keller M, Einloft J, Scharf KD, Schleiff E - Bioinform Biol Insights (2015)

The expression profile of RBF encoded by multiple genes. The expression values (Supplementary Table 4) for genes coding for RBFs with multiple co-orthologs have been normalized to the individual maximal value given next to the panel and the expression profile is shown (scale on the right). The order of samples is indicated on the right, legend in bold indicates the MACE results; the rest of the samples are derived from the NGS data.33Abbreviations: fmg: fruit mature green; fb: fruit breaker; fr: fruit ripe.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4325683&req=5

f9-bbi-9-2015-001: The expression profile of RBF encoded by multiple genes. The expression values (Supplementary Table 4) for genes coding for RBFs with multiple co-orthologs have been normalized to the individual maximal value given next to the panel and the expression profile is shown (scale on the right). The order of samples is indicated on the right, legend in bold indicates the MACE results; the rest of the samples are derived from the NGS data.33Abbreviations: fmg: fruit mature green; fb: fruit breaker; fr: fruit ripe.
Mentions: In general, about 25% of all RBFs predicted in A. thaliana and tomato are encoded by at least two different genes, which applies for all complexes involved in ribosome biogenesis (Figs. 2–4). The genes coding for RBFs are more strongly expressed in anther compared to leaf (Fig. 6; Table 3), which is not surprising, considering that anther is a male reproductive organ undergoing rapid metabolic changes. However, we also observed genes that show a stronger expression in leaves. These are mostly RBFs represented by multiple co-orthologs (Table 3), which is a hint for a tissue-specific set of assembly factors for ribosome biogenesis. In-depth analysis of the expression pattern of tomato RBFs with multiple co-orthologs in different tissues revealed differential expression for all (Fig. 9). Thus, we can conclude that the co-orthologs to individual RBFs found in plants account for a preferential expression in distinct tissues or at different developmental stages. This is consistent with the observed variation of the number of RBFs to which co-orthologs could be assigned (Fig. 2B). We conclude that plant ribosome biogenesis requires the action of tissue- or developmental stage-specific factors, which is in agreement with reports showing tissue-specific developmental defects in some RBF mutants.16,17,19,39 On the other hand, considering the critical function of individual RBFs for a vital cellular process like ribosome biogenesis, we can assume that other proteins with similar functions might compensate for the factors not predicted in any plant, a hypothesis that needs to be experimentally challenged in the future. On the other hand, the absence of some factors in plants might be explained by differences in the processing pathway compared to yeast, since for example, not all cleavage sites on plant rRNA have been mapped so far.

Bottom Line: In combination with existing expression profiles, we can conclude that co-orthologs of RBFs by large account for a preferential function in different tissue or at distinct developmental stages.In addition, co-regulated clusters of RBF and RP coding genes have been observed.The relevance of these results is discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, Frankfurt/Main, Germany. ; Cluster of Excellence Frankfurt, Goethe University, Frankfurt/Main, Germany.

ABSTRACT
Ribosome biogenesis involves a large inventory of proteinaceous and RNA cofactors. More than 250 ribosome biogenesis factors (RBFs) have been described in yeast. These factors are involved in multiple aspects like rRNA processing, folding, and modification as well as in ribosomal protein (RP) assembly. Considering the importance of RBFs for particular developmental processes, we examined the complexity of RBF and RP (co-)orthologs by bioinformatic assignment in 14 different plant species and expression profiling in the model crop Solanum lycopersicum. Assigning (co-)orthologs to each RBF revealed that at least 25% of all predicted RBFs are encoded by more than one gene. At first we realized that the occurrence of multiple RBF co-orthologs is not globally correlated to the existence of multiple RP co-orthologs. The transcript abundance of genes coding for predicted RBFs and RPs in leaves and anthers of S. lycopersicum was determined by next generation sequencing (NGS). In combination with existing expression profiles, we can conclude that co-orthologs of RBFs by large account for a preferential function in different tissue or at distinct developmental stages. This notion is supported by the differential expression of selected RBFs during male gametophyte development. In addition, co-regulated clusters of RBF and RP coding genes have been observed. The relevance of these results is discussed.

No MeSH data available.