TY - JOUR A1 - Trost, Gerda A1 - Vi, Son Lang A1 - Czesnick, Hjördis A1 - Lange, Peggy A1 - Holton, Nick A1 - Giavalisco, Patrick A1 - Zipfel, Cyril A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Arabidopsis poly(A) polymerase PAPS1 limits founder-cell recruitment to organ primordia and suppresses the salicylic acid-independent immune response downstream of EDS1/PAD4 JF - The plant journal N2 - Polyadenylation of pre-mRNAs by poly(A) polymerase (PAPS) is a critical process in eukaryotic gene expression. As found in vertebrates, plant genomes encode several isoforms of canonical nuclear PAPS enzymes. In Arabidopsis thaliana these isoforms are functionally specialized, with PAPS1 affecting both organ growth and immune response, at least in part by the preferential polyadenylation of subsets of pre-mRNAs. Here, we demonstrate that the opposite effects of PAPS1 on leaf and flower growth reflect the different identities of these organs, and identify a role for PAPS1 in the elusive connection between organ identity and growth patterns. The overgrowth of paps1 mutant petals is due to increased recruitment of founder cells into early organ primordia, and suggests that PAPS1 activity plays unique roles in influencing organ growth. By contrast, the leaf phenotype of paps1 mutants is dominated by a constitutive immune response that leads to increased resistance to the biotrophic oomycete Hyaloperonospora arabidopsidis and reflects activation of the salicylic acid-independent signalling pathway downstream of ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1)/PHYTOALEXIN DEFICIENT4 (PAD4). These findings provide an insight into the developmental and physiological basis of the functional specialization amongst plant PAPS isoforms. KW - poly(A) polymerase KW - founder-cell recruitment KW - organ growth KW - polyadenylation Y1 - 2014 U6 - https://doi.org/10.1111/tpj.12421 SN - 0960-7412 SN - 1365-313X VL - 77 IS - 5 SP - 688 EP - 699 PB - Wiley-Blackwell CY - Hoboken ER - TY - JOUR A1 - Vi, Son Lang A1 - Trost, Gerda A1 - Lange, Peggy A1 - Czesnick, Hjördis A1 - Rao, Nishta A1 - Lieber, Diana A1 - Laux, Thomas A1 - Gray, William M. A1 - Manley, James L. A1 - Groth, Detlef A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response JF - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA N2 - Polyadenylation of pre-mRNAs is critical for efficient nuclear export, stability, and translation of the mature mRNAs, and thus for gene expression. The bulk of pre-mRNAs are processed by canonical nuclear poly(A) polymerase (PAPS). Both vertebrate and higher-plant genomes encode more than one isoform of this enzyme, and these are coexpressed in different tissues. However, in neither case is it known whether the isoforms fulfill different functions or polyadenylate distinct subsets of pre-mRNAs. Here we show that the three canonical nuclear PAPS isoforms in Arabidopsis are functionally specialized owing to their evolutionarily divergent C-terminal domains. A strong loss-of-function mutation in PAPS1 causes a male gametophytic defect, whereas a weak allele leads to reduced leaf growth that results in part from a constitutive pathogen response. By contrast, plants lacking both PAPS2 and PAPS4 function are viable with wild-type leaf growth. Polyadenylation of SMALL AUXIN UP RNA (SAUR) mRNAs depends specifically on PAPS1 function. The resulting reduction in SAUR activity in paps1 mutants contributes to their reduced leaf growth, providing a causal link between polyadenylation of specific pre-mRNAs by a particular PAPS isoform and plant growth. This suggests the existence of an additional layer of regulation in plant and possibly vertebrate gene expression, whereby the relative activities of canonical nuclear PAPS isoforms control de novo synthesized poly(A) tail length and hence expression of specific subsets of mRNAs. Y1 - 2013 U6 - https://doi.org/10.1073/pnas.1303967110 SN - 0027-8424 VL - 110 IS - 34 SP - 13994 EP - 13999 PB - NATL ACAD SCIENCES CY - WASHINGTON ER - TY - JOUR A1 - Kappel, Christian A1 - Trost, Gerda A1 - Czesnick, Hjördis A1 - Ramming, Anna A1 - Kolbe, Benjamin A1 - Vi, Son Lang A1 - Bispo, Claudia A1 - Becker, Jörg D. A1 - de Moor, Cornelia A1 - Lenhard, Michael T1 - Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana JF - PLoS Genetics : a peer-reviewed, open-access journal N2 - 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. Y1 - 2015 U6 - https://doi.org/10.1371/journal.pgen.1005474 SN - 1553-7390 SN - 1553-7404 VL - 11 IS - 8 PB - PLoS CY - San Fransisco ER - TY - JOUR A1 - Kappel, Christian A1 - Trost, Gerda A1 - Czesnick, Hjördis A1 - Ramming, Anna A1 - Kolbe, Benjamin A1 - Vi, Son Lang A1 - Bispo, Cláudia A1 - Becker, Jörg D. A1 - de Moor, Cornelia A1 - Lenhard, Michael T1 - Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana JF - PLoS Genetics : a peer-reviewed, open-access journal N2 - 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. KW - messenger-rna polyadenylation KW - differential expression analysis KW - gene-expression KW - tail-length KW - cytoplasmic polyadenylation KW - poly(a)-binding protein KW - translational control KW - comprehensive analysis KW - specificity factor KW - mammalian-cells Y1 - 2015 U6 - https://doi.org/10.1371/journal.pgen.1005474 SN - 1553-7390 SN - 1553-7404 VL - 11 IS - 8 PB - Public Library of Science CY - San Francisco ER -