title: Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response.
abstract: 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.
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam, Germany.
authors.forename: Son Lang
authors.initials: SL
authors.lastname: Vi
authors.forename: Gerda
authors.initials: G
authors.lastname: Trost
authors.forename: Peggy
authors.initials: P
authors.lastname: Lange
authors.forename: Hjördis
authors.initials: H
authors.lastname: Czesnick
authors.forename: Nishta
authors.initials: N
authors.lastname: Rao
authors.forename: Diana
authors.initials: D
authors.lastname: Lieber
authors.forename: Thomas
authors.initials: T
authors.lastname: Laux
authors.forename: William M
authors.initials: WM
authors.lastname: Gray
authors.forename: James L
authors.initials: JL
authors.lastname: Manley
authors.forename: Detlef
authors.initials: D
authors.lastname: Groth
authors.forename: Christian
authors.initials: C
authors.lastname: Kappel
authors.forename: Michael
authors.initials: M
authors.lastname: Lenhard
mesh_terms: D021581:Active Transport, Cell Nucleus / Q000502:physiology*; D017360:Arabidopsis / Q000201:enzymology* / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D005838:Genotype; D046228:Microarray Analysis; D009154:Mutation / Q000235:genetics; D018515:Plant Leaves / Q000254:growth & development; D011062:Polynucleotide Adenylyltransferase / Q000235:genetics / Q000378:metabolism*; D012322:RNA Precursors / Q000378:metabolism*; D012333:RNA, Messenger / Q000235:genetics; D060888:Real-Time Polymerase Chain Reaction; D013379:Substrate Specificity
chemical_list: D029681:Arabidopsis Proteins; D012322:RNA Precursors; D012333:RNA, Messenger; C086789:SAUR-AC1 protein, Arabidopsis; D011062:Polynucleotide Adenylyltransferase
references.citation: Plant J. 2010 Jan;61(1):166-75
references.pmid: 19811619
references.citation: Plant J. 1998 Dec;16(6):735-43
references.pmid: 10069079
references.citation: J Biol Chem. 2001 Sep 7;276(36):33504-11
references.pmid: 11431479
references.citation: RNA. 2005 Jul;11(7):1131-40
references.pmid: 15929942
references.citation: Wiley Interdiscip Rev RNA. 2011 May-Jun;2(3):348-61
references.pmid: 21957022
references.citation: Plant Mol Biol. 2002 Jun-Jul;49(3-4):373-85
references.pmid: 12036261
references.citation: Curr Biol. 2006 Feb 7;16(3):272-9
references.pmid: 16461280
references.citation: Nucleic Acids Res. 2007;35(19):e132
references.pmid: 17933768
references.citation: Plant J. 2012 Jun;70(6):978-90
references.pmid: 22348445
references.citation: Mol Cell. 2011 Sep 16;43(6):853-66
references.pmid: 21925375
references.citation: Cell. 1995 May 5;81(3):379-89
references.pmid: 7736590
references.citation: PLoS One. 2009 Nov 26;4(11):e8082
references.pmid: 19956626
references.citation: Curr Top Microbiol Immunol. 2008;326:151-77
references.pmid: 18630752
references.citation: Nature. 2008 Feb 21;451(7181):1013-7
references.pmid: 18288197
references.citation: Genes Dev. 2011 Sep 1;25(17):1770-82
references.pmid: 21896654
references.citation: Nat Struct Mol Biol. 2012 Aug;19(8):845-52
references.pmid: 22820990
references.citation: RNA. 2007 Nov;13(11):1834-49
references.pmid: 17872511
references.citation: Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):979-83
references.pmid: 8302877
references.citation: Wiley Interdiscip Rev RNA. 2010 Jul-Aug;1(1):142-51
references.pmid: 21956911
references.citation: Plant J. 2001 May;26(4):409-20
references.pmid: 11439128
references.citation: Nature. 1991 Sep 19;353(6341):229-34
references.pmid: 1896071
references.citation: Science. 2010 Jan 1;327(5961):94-7
references.pmid: 19965720
references.citation: Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):7028-33
references.pmid: 19372383
references.citation: Plant Methods. 2011 Mar 13;7:7
references.pmid: 21396125
references.citation: Biochim Biophys Acta. 2004 Aug 12;1679(2):117-28
references.pmid: 15297145
references.citation: Cell Mol Life Sci. 2008 Apr;65(7-8):1099-122
references.pmid: 18158581
references.citation: Curr Opin Plant Biol. 2004 Oct;7(5):547-52
references.pmid: 15337097
references.citation: Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):8943-8
references.pmid: 10430875
references.citation: Science. 2002 Dec 6;298(5600):1999-2002
references.pmid: 12471261
references.citation: Cell. 1988 Mar 11;52(5):731-42
references.pmid: 2830992
references.citation: Nucleic Acids Res. 2010 Jan;38(Database issue):D828-34
references.pmid: 19880383
references.citation: Mol Cell Biol. 2001 Aug;21(16):5614-23
references.pmid: 11463842
references.citation: Plant J. 2006 Nov;48(4):638-44
references.pmid: 17076802
references.citation: Nucleic Acids Res. 2010 May;38(9):2757-74
references.pmid: 20044349
references.citation: Nature. 1991 Dec 12;354(6353):496-8
references.pmid: 1840648
references.citation: Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13991-6
references.pmid: 11087822
references.citation: Biochem Biophys Res Commun. 2000 May 27;272(1):174-81
references.pmid: 10872823
references.citation: BMC Genomics. 2008 May 14;9:220
references.pmid: 18479511
references.citation: Dev Biol. 2001 May 1;233(1):137-47
references.pmid: 11319863
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12533-8
references.pmid: 21746925
references.citation: EMBO J. 2002 Dec 2;21(23):6603-13
references.pmid: 12456666
references.citation: Plant J. 2012 Aug;71(4):684-97
references.pmid: 22507274
references.citation: Stat Appl Genet Mol Biol. 2004;3:Article3
references.pmid: 16646809
references.citation: Mol Cell Biol. 1996 May;16(5):2378-86
references.pmid: 8628305
references.citation: Methods. 2003 Dec;31(4):265-73
references.pmid: 14597310
references.citation: Plant Cell. 1994 Dec;6(12):1845-57
references.pmid: 7866028
references.citation: Science. 2008 Jun 20;320(5883):1643-7
references.pmid: 18566288