Home LiteratureArticle Details
PMID: 27726481 Published · ppublish English Journal Article Review Research Support, Non-U.S. Gov't

Cajal bodies and their role in plant stress and disease responses.

RNA biology ·Vol. 14 ·No. 6 ·2017-00-03 ·Pages 779-790

Love AJ, Yu C, Petukhova NV, Kalinina NO, Chen J, Taliansky ME

Abstract

Cajal bodies (CBs) are distinct sub-nuclear structures that are present in eukaryotic living cells and are often associated with the nucleolus. CBs play important roles in RNA metabolism and formation of RNPs involved in transcription, splicing, ribosome biogenesis, and telomere maintenance. Besides these primary roles, CBs appear to be involved in additional functions that may not be directly related to RNA metabolism and RNP biogenesis. In this review, we assess possible roles of plant CBs in RNA regulatory pathways such as nonsense-mediated mRNA decay and RNA silencing. We also summarize recent progress and discuss new non-canonical functions of plant CBs in responses to stress and disease. It is hypothesized that CBs can regulate these responses via their interaction with poly(ADP ribose)polymerase (PARP), which is known to play an important role in various physiological processes including responses to biotic and abiotic stresses. It is suggested that CBs and their components modify PARP activities and functions.

Keywords
Abiotic stress Cajal bodies PARP plant viruses plants
MeSH Terms
Coiled Bodies/genetics,metabolism Gene Expression Regulation, Plant Host-Pathogen Interactions/genetics Nuclear Proteins/metabolism Plant Diseases/genetics,virology Plant Physiological Phenomena Poly(ADP-ribose) Polymerases/metabolism RNA Processing, Post-Transcriptional RNA, Small Nuclear/genetics,metabolism Ribonucleoproteins, Small Nuclear/metabolism Stress, Physiological/genetics
Chemicals
Nuclear Proteins RNA, Small Nuclear Ribonucleoproteins, Small Nuclear p80-coilin Poly(ADP-ribose) Polymerases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Love Andrew J
a Cell and Molecular Sciences , James Hutton Institute , Invergowrie, Dundee , UK.
Yu Chulang
b State Key Laboratory Breeding Base for Sustainable Pest and Disease Control, Key Laboratory of Biotechnology in Plant Protection of MOA and Zhejiang Province , Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences , Hangzhou , China.
Petukhova Natalia V
a Cell and Molecular Sciences , James Hutton Institute , Invergowrie, Dundee , UK.
Kalinina Natalia O
c A.N. Belozersky Institute of Physico-Chemical Biology , Lomonosov Moscow State University , Leninskie Gory, Moscow , Russia.
Chen Jianping
b State Key Laboratory Breeding Base for Sustainable Pest and Disease Control, Key Laboratory of Biotechnology in Plant Protection of MOA and Zhejiang Province , Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences , Hangzhou , China.
Taliansky Michael E
a Cell and Molecular Sciences , James Hutton Institute , Invergowrie, Dundee , UK. | b State Key Laboratory Breeding Base for Sustainable Pest and Disease Control, Key Laboratory of Biotechnology in Plant Protection of MOA and Zhejiang Province , Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences , Hangzhou , China.
References (111)
111 references, click to expand
  1. Cajal bodies: a long history of discovery.
    Annu Rev Cell Dev Biol. 2005;21:105-31 PMID: 16212489
  2. A common sequence motif determines the Cajal body-specific localization of box H/ACA scaRNAs.
    EMBO J. 2003 Aug 15;22(16):4283-93 PMID: 12912925
  3. Phosphorylation regulates coilin activity and RNA association.
    Biol Open. 2013 Feb 26;2(4):407-15 PMID: 23616925
  4. Periodic expression of Sm proteins parallels formation of nuclear Cajal bodies and cytoplasmic snRNP-rich bodies.
    Histochem Cell Biol. 2011 Nov;136(5):527-41 PMID: 21904826
  5. Cajal body surveillance of U snRNA export complex assembly.
    J Cell Biol. 2010 Aug 23;190(4):603-12 PMID: 20733056
  6. Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis to biotic stress.
    Plant Physiol. 2010 Jan;152(1):267-80 PMID: 19889874
  7. The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants.
    FEBS Lett. 1998 Nov 27;440(1-2):1-7 PMID: 9862413
  8. Form, function, and regulation of ARGONAUTE proteins.
    Plant Cell. 2010 Dec;22(12):3879-89 PMID: 21183704
  9. A plant virus-encoded protein facilitates long-distance movement of heterologous viral RNA.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1212-7 PMID: 9990003
  10. UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis.
    Plant J. 2006 Aug;47(3):480-9 PMID: 16813578
  11. The coilin interactome identifies hundreds of small noncoding RNAs that traffic through Cajal bodies.
    Mol Cell. 2014 Nov 6;56(3):389-99 PMID: 25514182
  12. De novo formation of a subnuclear body.
    Science. 2008 Dec 12;322(5908):1713-7 PMID: 18948503
  13. Umbravirus-encoded proteins both stabilize heterologous viral RNA and mediate its systemic movement in some plant species.
    Virology. 2001 Sep 30;288(2):391-400 PMID: 11601910
  14. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis.
    Nat Struct Mol Biol. 2010 Apr;17(4):403-9 PMID: 20357773
  15. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1.
    Genes Dev. 2012 Mar 1;26(5):417-32 PMID: 22391446
  16. Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana.
    J Biol Chem. 2000 Sep 1;275(35):27212-20 PMID: 10829025
  17. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis.
    Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):3145-50 PMID: 18287047
  18. Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells.
    FEBS Lett. 2000 May 26;474(1):11-5 PMID: 10828442
  19. Intracellular location of two groundnut rosette umbravirus proteins delivered by PVX and TMV vectors.
    Virology. 1998 Mar 15;242(2):303-13 PMID: 9514976
  20. Cajal bodies: where form meets function.
    Wiley Interdiscip Rev RNA. 2013 Jan-Feb;4(1):17-34 PMID: 23042601
  21. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence.
    Nat Rev Microbiol. 2013 Nov;11(11):745-60 PMID: 24129510
  22. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center.
    Cell. 2006 Jul 14;126(1):79-92 PMID: 16839878
  23. Aberrant mRNA transcripts and the nonsense-mediated decay proteins UPF2 and UPF3 are enriched in the Arabidopsis nucleolus.
    Plant Cell. 2009 Jul;21(7):2045-57 PMID: 19602621
  24. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin.
    PLoS One. 2009 Jul 09;4(7):e6171 PMID: 19587784
  25. Poly(ADP-ribosyl)ation in plants.
    Trends Plant Sci. 2011 Jul;16(7):372-80 PMID: 21482174
  26. Control of Cajal body number is mediated by the coilin C-terminus.
    J Cell Sci. 2003 Jan 15;116(Pt 2):303-12 PMID: 12482916
  27. An umbraviral protein, involved in long-distance RNA movement, binds viral RNA and forms unique, protective ribonucleoprotein complexes.
    J Virol. 2003 Mar;77(5):3031-40 PMID: 12584328
  28. Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions.
    Mol Biol Cell. 2005 Jan;16(1):260-9 PMID: 15496452
  29. Cajal body-specific small nuclear RNAs: a novel class of 2'-O-methylation and pseudouridylation guide RNAs.
    EMBO J. 2002 Jun 3;21(11):2746-56 PMID: 12032087
  30. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus.
    J Cell Biol. 1995 Nov;131(4):817-31 PMID: 7490287
  31. Dicing bodies.
    Plant Physiol. 2012 Jan;158(1):61-6 PMID: 22025607
  32. Direct interaction of the spinal muscular atrophy disease protein SMN with the small nucleolar RNA-associated protein fibrillarin.
    J Biol Chem. 2001 Oct 19;276(42):38645-51 PMID: 11509571
  33. Biogenesis of small nuclear RNPs.
    J Cell Sci. 2004 Dec 1;117(Pt 25):5949-51 PMID: 15564372
  34. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage.
    Mol Cell Proteomics. 2010 Mar;9(3):457-70 PMID: 20026476
  35. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product.
    J Cell Biol. 2001 Jul 23;154(2):293-307 PMID: 11470819
  36. Molecular mechanism of action of plant DRM de novo DNA methyltransferases.
    Cell. 2014 May 22;157(5):1050-60 PMID: 24855943
  37. Poly(A) RNAs including coding proteins RNAs occur in plant Cajal bodies.
    PLoS One. 2014 Nov 04;9(11):e111780 PMID: 25369024
  38. Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance.
    Mol Cell Biol. 2008 Apr;28(7):2332-41 PMID: 18212040
  39. Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body.
    Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5437-42 PMID: 17369351
  40. State of the arg: protein methylation at arginine comes of age.
    Cell. 2001 Jul 13;106(1):5-8 PMID: 11461695
  41. Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body.
    PLoS Genet. 2009 Feb;5(2):e1000387 PMID: 19229318
  42. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus.
    Exp Cell Res. 1997 Jan 10;230(1):84-93 PMID: 9013710
  43. RNA polymerase V transcription guides ARGONAUTE4 to chromatin.
    Nat Genet. 2009 May;41(5):630-4 PMID: 19377477
  44. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana.
    Cell. 2006 Jul 14;126(1):93-106 PMID: 16839879
  45. The spliceosome assembly factor GEMIN2 attenuates the effects of temperature on alternative splicing and circadian rhythms.
    Proc Natl Acad Sci U S A. 2015 Jul 28;112(30):9382-7 PMID: 26170331
  46. Getting the message across: how do plant cells exchange macromolecular complexes?
    Trends Plant Sci. 2004 Jan;9(1):33-41 PMID: 14729217
  47. Coilin methylation regulates nuclear body formation.
    Dev Cell. 2002 Sep;3(3):329-37 PMID: 12361597
  48. Location of a possible miRNA processing site in SmD3/SmB nuclear bodies in Arabidopsis.
    Plant Cell Physiol. 2007 Sep;48(9):1243-53 PMID: 17675322
  49. Cajal-body formation correlates with differential coilin phosphorylation in primary and transformed cell lines.
    J Cell Sci. 2009 Jun 1;122(Pt 11):1872-81 PMID: 19435804
  50. Small Cajal body-specific RNAs of Drosophila function in the absence of Cajal bodies.
    Mol Biol Cell. 2009 Dec;20(24):5250-9 PMID: 19846657
  51. Nucleation of nuclear bodies by RNA.
    Nat Cell Biol. 2011 Feb;13(2):167-73 PMID: 21240286
  52. The movement of coiled bodies visualized in living plant cells by the green fluorescent protein.
    Mol Biol Cell. 1999 Jul;10(7):2297-307 PMID: 10397766
  53. Involvement of the nucleolus in replication of human viruses.
    Rev Med Virol. 2009 Jul;19(4):201-14 PMID: 19399920
  54. Evolution of an RNP assembly system: a minimal SMN complex facilitates formation of UsnRNPs in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):10045-50 PMID: 18621711
  55. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes.
    Virology. 2006 Jan 5;344(1):169-84 PMID: 16364748
  56. Coilin: The first 25 years.
    RNA Biol. 2015;12(6):590-6 PMID: 25970135
  57. Interferon-stimulated poly(ADP-Ribose) polymerases are potent inhibitors of cellular translation and virus replication.
    J Virol. 2014 Feb;88(4):2116-30 PMID: 24335297
  58. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm.
    EMBO J. 2003 Apr 15;22(8):1878-88 PMID: 12682020
  59. Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana.
    Curr Biol. 2002 Dec 10;12(23):2002-13 PMID: 12477388
  60. Telomere- and Telomerase-Associated Proteins and Their Functions in the Plant Cell.
    Front Plant Sci. 2016 Jun 28;7:851 PMID: 27446102
  61. Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata.
    J Exp Bot. 2009;60(3):939-54 PMID: 19213813
  62. RNA interference in pigs: comparison of RNAi test systems and expression vectors.
    Mol Biotechnol. 2011 May;48(1):38-48 PMID: 21057895
  63. The Drosophila melanogaster Cajal body.
    J Cell Biol. 2006 Mar 13;172(6):875-84 PMID: 16533947
  64. Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana.
    PLoS Genet. 2008 Feb;4(2):e27 PMID: 18266474
  65. Plant coilin: structural characteristics and RNA-binding properties.
    PLoS One. 2013;8(1):e53571 PMID: 23320094
  66. Involvement of the plant nucleolus in virus and viroid infections: parallels with animal pathosystems.
    Adv Virus Res. 2010;77:119-58 PMID: 20951872
  67. A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis.
    Mol Biol Cell. 2006 Jul;17(7):2942-51 PMID: 16624863
  68. Nucleolar proteome dynamics.
    Nature. 2005 Jan 6;433(7021):77-83 PMID: 15635413
  69. Large-scale isolation of Cajal bodies from HeLa cells.
    Mol Biol Cell. 2002 Jul;13(7):2461-73 PMID: 12134083
  70. Self-association of coilin reveals a common theme in nuclear body localization.
    Mol Biol Cell. 2000 Dec;11(12):4159-71 PMID: 11102515
  71. Is the sphere organelle/coiled body a universal nuclear component?
    Dev Genet. 1995;16(1):25-35 PMID: 7758244
  72. Cajal bodies and the nucleolus are required for a plant virus systemic infection.
    EMBO J. 2007 Apr 18;26(8):2169-79 PMID: 17410203
  73. Movement protein of hordeivirus interacts in vitro and in vivo with coilin, a major structural protein of Cajal bodies.
    Dokl Biochem Biophys. 2012 Jan-Feb;442:57-60 PMID: 22419098
  74. UPF3 suppresses aberrant spliced mRNA in Arabidopsis.
    Plant J. 2005 Aug;43(4):530-40 PMID: 16098107
  75. Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins.
    Int J Mol Sci. 2013 Aug 05;14(8):16168-83 PMID: 23921685
  76. Cajal bodies and coilin--moving towards function.
    J Cell Biol. 2002 Oct 14;159(1):17-21 PMID: 12379800
  77. Association of the neuron-specific RNA binding domain-containing protein ELAV with the coiled body in Drosophila neurons.
    Chromosoma. 1997 Apr;105(6):332-41 PMID: 9087375
  78. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies.
    Exp Cell Res. 1991 Jul;195(1):27-37 PMID: 2055273
  79. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes.
    Cell. 2008 Nov 14;135(4):635-48 PMID: 19013275
  80. Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1947-51 PMID: 8446613
  81. Coilin, the signature protein of Cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa.
    Nucleus. 2014 Jan-Feb;5(1):85-94 PMID: 24637832
  82. Poly(ADP-ribose)polymerase activity controls plant growth by promoting leaf cell number.
    PLoS One. 2014 Feb 28;9(2):e90322 PMID: 24587323
  83. Activation of the programmed cell death pathway by inhibition of proteasome function in plants.
    J Biol Chem. 2003 May 23;278(21):19406-15 PMID: 12637532
  84. Pumping RNA: nuclear bodybuilding along the RNP pipeline.
    Curr Opin Cell Biol. 2006 Jun;18(3):317-24 PMID: 16632338
  85. Coilin is essential for Cajal body organization in Drosophila melanogaster.
    Mol Biol Cell. 2009 Mar;20(6):1661-70 PMID: 19158395
  86. Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis--evidence that the coiled body is a kinetic nuclear structure.
    J Cell Biol. 1993 Feb;120(4):841-52 PMID: 7679389
  87. The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze.
    Chromosoma. 2006 Oct;115(5):343-54 PMID: 16575476
  88. Identification of a nuclear localization signal and nuclear export signal of the umbraviral long-distance RNA movement protein.
    J Gen Virol. 2004 May;85(Pt 5):1329-33 PMID: 15105550
  89. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning.
    Nat Genet. 2006 Jun;38(6):721-5 PMID: 16699516
  90. Effects of cytosine methylation on transcription factor binding sites.
    BMC Genomics. 2014 Mar 26;15:119 PMID: 24669864
  91. Dynamic interactions between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein.
    Exp Cell Res. 1998 Sep 15;243(2):290-304 PMID: 9743589
  92. Biogenesis and function of nuclear bodies.
    Trends Genet. 2011 Aug;27(8):295-306 PMID: 21680045
  93. In vivo analysis of Cajal body movement, separation, and joining in live human cells.
    J Cell Biol. 2000 Dec 25;151(7):1561-74 PMID: 11134083
  94. RNA viruses: hijacking the dynamic nucleolus.
    Nat Rev Microbiol. 2007 Feb;5(2):119-27 PMID: 17224921
  95. A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrillarin, in vitro.
    J Mol Biol. 2008 Feb 29;376(4):932-7 PMID: 18199452
  96. The nucleolus under stress.
    Mol Cell. 2010 Oct 22;40(2):216-27 PMID: 20965417
  97. The organization of spliceosomal components in the nuclei of higher plants.
    J Cell Sci. 1995 Feb;108 ( Pt 2):509-18 PMID: 7768997
  98. Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection.
    Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):11115-20 PMID: 17576925
  99. PARP2 Is the Predominant Poly(ADP-Ribose) Polymerase in Arabidopsis DNA Damage and Immune Responses.
    PLoS Genet. 2015 May 07;11(5):e1005200 PMID: 25950582
  100. Poly(ADP-ribose) polymerase-1 silences retroviruses independently of viral DNA integration or heterochromatin formation.
    J Gen Virol. 2016 Jul;97(7):1686-92 PMID: 27028089
  101. Chaperones and multitasking proteins in the nucleolus: networking together for survival?
    Trends Biochem Sci. 2010 Jul;35(7):361-7 PMID: 20363631
  102. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin.
    J Exp Med. 1991 Jun 1;173(6):1407-19 PMID: 2033369
  103. Human p80-coilin is targeted to sphere organelles in the amphibian germinal vesicle.
    Mol Biol Cell. 1994 Oct;5(10):1119-27 PMID: 7532471
  104. Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells.
    J Cell Biol. 2001 Apr 2;153(1):169-76 PMID: 11285283
  105. Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine.
    Plant Cell. 2006 Oct;18(10):2767-81 PMID: 17041150
  106. The role of Cajal bodies in the expression of late phase adenovirus proteins.
    Virology. 2010 Apr 10;399(2):299-311 PMID: 20137801
  107. Dynamic organization of the cell nucleus.
    Curr Opin Genet Dev. 2007 Oct;17(5):373-80 PMID: 17913491
  108. Plant U13 orthologues and orphan snoRNAs identified by RNomics of RNA from Arabidopsis nucleoli.
    Nucleic Acids Res. 2010 May;38(9):3054-67 PMID: 20081206
  109. Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance.
    Plant J. 2005 Jan;41(1):95-106 PMID: 15610352
  110. Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of Soybean mosaic virus.
    Plant Cell Rep. 2012 May;31(5):905-16 PMID: 22200865
  111. The Cajal body.
    Biochim Biophys Acta. 2008 Nov;1783(11):2108-15 PMID: 18755223
Article Info
Journal
RNA biology
Abbr.
RNA Biol
ISSN
1555-8584
Published
2017-00-03
Epub
2016-00-11
Pages
779-790
Language
English
Region
United States
NLM ID
101235328
PMCID
PMC5519230
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com