Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana
The poly(A) tail at 3’ ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases,PAPS1, PAPS2 and PAPS4. As shown b...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Published: |
Public Library of Science
2015
|
| Online Access: | https://eprints.nottingham.ac.uk/37518/ |
| _version_ | 1848795476383498240 |
|---|---|
| author | Kappel, Christian Trost, Gerda Cseznick, Hjordis Ramming, Anna Kolbe, Benjamin Vi, Son Lang Becker, Jörg D. de Moor, Cornelia H. Lenhard, Michael |
| author_facet | Kappel, Christian Trost, Gerda Cseznick, Hjordis Ramming, Anna Kolbe, Benjamin Vi, Son Lang Becker, Jörg D. de Moor, Cornelia H. Lenhard, Michael |
| author_sort | Kappel, Christian |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | The poly(A) tail at 3’ ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases,PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptome-wide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale co-expression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression. |
| first_indexed | 2025-11-14T19:32:42Z |
| format | Article |
| id | nottingham-37518 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| last_indexed | 2025-11-14T19:32:42Z |
| publishDate | 2015 |
| publisher | Public Library of Science |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-375182020-05-04T17:14:42Z https://eprints.nottingham.ac.uk/37518/ Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana Kappel, Christian Trost, Gerda Cseznick, Hjordis Ramming, Anna Kolbe, Benjamin Vi, Son Lang Becker, Jörg D. de Moor, Cornelia H. Lenhard, Michael The poly(A) tail at 3’ ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases,PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptome-wide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale co-expression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression. Public Library of Science 2015-08-25 Article PeerReviewed Kappel, Christian, Trost, Gerda, Cseznick, Hjordis, Ramming, Anna, Kolbe, Benjamin, Vi, Son Lang, Becker, Jörg D., de Moor, Cornelia H. and Lenhard, Michael (2015) Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana. PLoS Genetics, 11 (8). e1005474/1-e1005474/30. ISSN 1553-7404 http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005474 doi:10.1371/journal.pgen.1005474 doi:10.1371/journal.pgen.1005474 |
| spellingShingle | Kappel, Christian Trost, Gerda Cseznick, Hjordis Ramming, Anna Kolbe, Benjamin Vi, Son Lang Becker, Jörg D. de Moor, Cornelia H. Lenhard, Michael Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title | Genome-wide analysis of PAPS1-dependent
polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title_full | Genome-wide analysis of PAPS1-dependent
polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title_fullStr | Genome-wide analysis of PAPS1-dependent
polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title_full_unstemmed | Genome-wide analysis of PAPS1-dependent
polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title_short | Genome-wide analysis of PAPS1-dependent
polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana |
| title_sort | genome-wide analysis of paps1-dependent
polyadenylation identifies novel roles for functionally specialized poly(a) polymerases in arabidopsis thaliana |
| url | https://eprints.nottingham.ac.uk/37518/ https://eprints.nottingham.ac.uk/37518/ https://eprints.nottingham.ac.uk/37518/ |