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Annual Plant Reviews, Volume 46Plant Nuclear Structure,Genome Architecture and Gene RegulationEdited by David E. Evans, Katja Graumann and John A. Bryant

ANNUAL PLANT REVIEWSVOLUME 46

ANNUAL PLANT REVIEWSVOLUME 46Plant Nuclear Structure,Genome Architectureand Gene RegulationEdited byDavid E. EvansDepartment of Biological and Medical SciencesOxford Brookes University, Oxford, UKKatja GraumannDepartment of Biological and Medical SciencesOxford Brookes University, Oxford, UKJohn A. BryantBiosciences, University of Exeter, Exeter, UKA John Wiley & Sons, Ltd., Publication

C 2013 by John Wiley & Sons, LtdThis edition first published 2013. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’sglobal Scientific, Technical and Medical business with Blackwell Publishing.Registered office: John Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester,West Sussex, PO19 8SQ, UKEditorial offices: 9600 Garsington Road, Oxford, OX4 2DQ, UKThe Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK111 River Street, Hoboken, NJ 07030-5774, USAFor details of our global editorial offices, for customer services and for information abouthow to apply for permission to reuse the copyright material in this book please see ourwebsite at www.wiley.com/wiley-blackwell.The right of the author to be identified as the author of this work has been asserted inaccordance with the UK Copyright, Designs and Patents Act 1988.All rights reserved. No part of this publication may be reproduced, stored in a retrievalsystem, or transmitted, in any form or by any means, electronic, mechanical,photocopying, recording or otherwise, except as permitted by the UK Copyright, Designsand Patents Act 1988, without the prior permission of the publisher.Designations used by companies to distinguish their products are often claimed astrademarks. All brand names and product names used in this book are trade names,service marks, trademarks or registered trademarks of their respective owners. Thepublisher is not associated with any product or vendor mentioned in this book.Limit of Liability/Disclaimer of Warranty: While the publisher and author(s) have usedtheir best efforts in preparing this book, they make no representations or warranties withrespect to the accuracy or completeness of the contents of this book and specificallydisclaim any implied warranties of merchantability or fitness for a particular purpose. Itis sold on the understanding that the publisher is not engaged in rendering professionalservices and neither the publisher nor the author shall be liable for damages arisingherefrom. If professional advice or other expert assistance is required, the services of acompetent professional should be sought.Library of Congress Cataloging-in-Publication Data has been applied forISBN 978-1-1184-7245-3 (hardback)A catalogue record for this book is available from the British Library.Wiley also publishes its books in a variety of electronic formats. Some content thatappears in print may not be available in electronic books.Cover image: Images supplied by Katja GraumannCover design by www.hisandhersdesign.co.ukRInc., New Delhi, IndiaSet in 10/12pt Palatino by Aptara First Impression 2013

Annual Plant ReviewsA series for researchers and postgraduates in the plant sciences. Each volumein this series focuses on a theme of topical importance and emphasis is placedon rapid publication.Editorial Board:Prof. Jeremy A. Roberts (Editor-in-Chief), Plant Science Division, School ofBiosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK;Prof. David E. Evans, Department of Biological and Medical Sciences, OxfordBrookes University, Headington Campus, Oxford OX3 0BP, UK;Dr Michael T. McManus, Institute of Molecular BioSciences, Massey University, Palmerston North, New Zealand;Dr Jocelyn K.C. Rose, Department of Plant Biology, Cornell University,Ithaca, New York 14853, USA.Titles in the series:1. ArabidopsisEdited by M. Anderson and J.A. Roberts2. Biochemistry of Plant Secondary MetabolismEdited by M. Wink3. Functions of Plant Secondary Metabolites and their Exploitation inBiotechnologyEdited by M. Wink4. Molecular Plant PathologyEdited by M. Dickinson and J. Beynon5. Vacuolar CompartmentsEdited by D.G. Robinson and J.C. Rogers6. Plant ReproductionEdited by S.D. O’Neill and J.A. Roberts7. Protein–Protein Interactions in Plant BiologyEdited by M.T. McManus, W.A. Laing and A.C. Allan8. The Plant CellWallEdited by J.K.C. Rose9. The Golgi Apparatus and the Plant Secretory PathwayEdited by D.G. Robinson10. The Plant Cytoskeleton in Cell Differentiation and DevelopmentEdited by P.J. Hussey11. Plant–Pathogen InteractionsEdited by N.J. Talbot12. Polarity in PlantsEdited by K. Lindsey13. PlastidsEdited by S.G. Moller14. Plant Pigments and their ManipulationEdited by K. Davies

15. Membrane Transport in PlantsEdited by M.R. Blatt16. Intercellular Communication in PlantsEdited by A.J. Fleming17. Plant Architecture and Its ManipulationEdited by C.G.N. Turnbull18. PlasmodeomataEdited by K.J. Oparka19. Plant EpigeneticsEdited by P. Meyer20. Flowering and Its ManipulationEdited by C. Ainsworth21. Endogenous Plant RhythmsEdited by A. Hall and H. McWatters22. Control of Primary Metabolism in PlantsEdited by W.C. Plaxton and M.T. McManus23. Biology of the Plant CuticleEdited by M. Riederer24. Plant Hormone SignalingEdited by P. Hadden and S.G. Thomas25. Plant Cell Separation and AdhesionEdited by J.R. Roberts and Z. Gonzalez-Carranza26. Senescence Processes in PlantsEdited by S. Gan27. Seed Development, Dormancy and GerminationEdited by K.J. Bradford and H. Nonogaki28. Plant ProteomicsEdited by C. Finnie29. Regulation of Transcription in PlantsEdited by K. Grasser30. Light and Plant DevelopmentEdited by G. Whitelam31. Plant MitochondriaEdited by D.C. Logan32. Cell Cycle Control and Plant DevelopmentEdited by D. Inzé33. Intracellular Signaling in PlantsEdited by Z. Yang34. Molecular Aspects of Plant Disease ResistanceEdited by J. Parker35. Plant Systems BiologyEdited by G.M. Coruzzi and R.A. Gutiérrez36. The Moss Physcomitrella patensEdited by C.D. Knight, P.-F. Perroud and D.J. Cove37. Root DevelopmentEdited by T. Beeckman38. Fruit Development and Seed DispersalEdited by L. Østergaard

39. Function and Biotechnology of Plant Secondary MetabolitesEdited by M. Wink40. Biochemistry of Plant Secondary MetabolismEdited by M. Wink41. Plant PolysaccharidesEdited by P. Ulvskov42. Nitrogen Metabolism in Plants in the Post-genomic EraEdited by C. Foyer and H. Zhang43. Biology of Plant MetabolomicsEdited by R.D. Hall44. The Plant Hormone EthyleneEdited by M.T. McManus45. The Evolution of Plant FormEdited by B.A. Ambrose and M.D. Purugganan

CONTENTSList of ContributorsPrefaceAcknowledgements1Introduction: Mysteries, Molecules and MechanismsJohn A. Bryant1.11.21.31.41.52Darwin and Margulis revisitedNuclei – general featuresThe plant nuclear genome1.3.1 General features1.3.2 Replication of the nuclear genomeDNA inside, ribosomes outsideConcluding comments on the evolution of the nucleusReferencesxvxixxxiii11355691113The Nuclear Envelope – Structure and Protein InteractionsKatja Graumann and David E. ctionOrganization and structure of the plant nuclear envelopeProteins of the plant nuclear envelope2.3.1 Proteins involved in signalling2.3.2 Proteins of the nuclear pore complex2.3.3 Proteins of the INM2.3.4 Proteins spanning the periplasm and linkingthe NE membranes2.3.5 The plant laminaThe plant nuclear envelope and the nucleoskeleton;attachments at the INMThe plant nuclear envelope and the cytoskeleton;attachments at the ONMTargeting of proteins to the plant NENuclear envelope protein dynamics in mitosis2.7.1 The role of NPC in regulating NE dynamics incell division2.7.2 NE protein dynamics in divisionThe phragmoplast and cell plate and their relationshipto the NE252831353638384041ix

x Contents2.9 The plant NE in meiosis2.10 Lipid composition of the plant NE and its homeostasis2.10.1 Nuclear-vacuolar junctions and lipid homeostasis2.10.2 NE phospholipid regulation by lipins2.11 The role of plant NE components in stress responses2.11.1 Nuclei repositioning in response toenvironmental stimuli2.11.2 Functions of the plant NE during viral infection2.12 Concluding remarksReferences3 The Plant Nuclear Pore Complex – The NucleocytoplasmicBarrier and BeyondXiao Zhou, Joanna Boruc and Iris Meier3.1 Nuclear pore complex structure3.1.1Structure of the NPC3.1.2Molecular composition of the NPC3.1.3Nucleocytoplasmic trafficking3.2 Physiological and developmental roles of plant nuclearpore components3.2.1Plant–microbe interactions3.2.2Hormone responses3.2.3Abiotic stress responses3.2.4Growth and development3.3 The Dynamics of the Nuclear Pore Complex3.3.1Types of mitosis3.3.2NPC disassembly and dynamics of animal NPCcomponents3.3.3Dynamics of fungal NPC components3.3.4Dynamics of plant NPC components3.4 ConclusionsReferences4 Nucleoskeleton in Plants: The Functional Organization ofFilaments in the NucleusMartin W. Goldberg4.1 Introduction4.2 Intermediate filaments and the nucleoskeleton4.3 Plants do not have intermediate filaments but they mayhave functional equivalents4.4 Plants can evolve different solutions to the same problem4.5 Intermediate filaments first evolved in the nucleus4.6 Plants require a rigid nuclear 767879818193949699100101101

Contents 8109109112113113114Genomics and Chromatin PackagingEugenio 455.35.45.56Is there a trans-nuclear envelope complex in plants thatlinks the nucleoskeleton to the cytoskeleton?Role of the nuclear lamina as part of the nucleoskeletonStructural evidence for the nucleoskeletonNuMA in plantsMatrix attachment regions (MARs) and the role of thenucleoskeleton in chromatin organizationChromocentres and the plant nucleoskeletonLong coiled-coil proteins in plants and their role in nuclearorganization: candidates for plamins and nucleoskeletalproteins?Actin and microtubules in the tin components and structure in higher eukaryotesHistones and nucleosome fibre5.2.1 Histone variants5.2.2 Histone modifications5.2.3 Nucleosome dynamicsLinker histone and the higher order chromatin-order fibre5.3.1 The elusive higher order chromatin fibreChromatin loops and chromosome axisConclusions and future prospectsReferencesHeterochromatin Positioning and Nuclear ArchitectureEmmanuel Vanrobays, Mélanie Thomas and Christophe Tatout6.1 Heterochromatin structure6.1.1 Heterochromatic sequences6.1.2 Epigenetic marks6.1.3 Non-histone protein binding6.1.4 Heterochromatin is an epigenetic state6.2 Heterochromatin organization6.2.1 Heterochromatin and nuclear architecture6.2.2 Recruitment of heterochromatin at the nuclearperiphery6.2.3 Higher order of chromatin organization6.3 Functional significance of heterochromatin positioning6.3.1 Centric heterochromatin directs 3176176

xii Contents6.3.26.4Spatial positioning of heterochromatin affectstranscriptional activity6.3.3Heterochromatin positioning protectsagainst genome instabilityPerspectivesAcknowledgementsReferences7 Telomeres in Plant Meiosis: Their Structure, Dynamicsand FunctionNicola Y. Roberts, Kim Osman, F. Chris H. Franklin, Monica Pradillo,Javier Varas, Juan L. Santos and Susan J. Armstrong7.1 Introduction7.1.1The meiotic pathway7.1.2Arabidopsis thaliana as a model for meiosis7.2 The telomeres and associated proteins7.2.1Telomere binding proteins7.2.2Arabidopsis telomere binding proteins7.2.3DNA repair proteins7.3 The behaviour of the telomeres in meiosis7.3.1The bouquet7.3.2A role for the bouquet7.4 Telomere dynamics in Arabidopsis thaliana meiosis7.4.1Meiosis in A. thaliana telomere-deficient lines7.5 How are the telomeres moved in meiotic prophase I?7.5.1Colchicine disrupts meiotic progression7.5.2The role of actin in telomere movement7.6 Components of the nuclear envelope7.7 Components of the plant nuclear envelope7.8 Conclusions and future prospectsAcknowledgementsReferences8 The Nuclear Pore Complex in Symbiosis and Pathogen DefenceAndreas Binder and Martin Parniske8.1 Introduction8.2 The nuclear pore and plant-microbe symbiosis8.2.1Common signalling in arbuscular mycorrhiza androot-nodule symbiosis8.2.2Symbiotic signalling at the nucleus8.2.3Symbiotic defects in ljnup85, ljnup133 and 0231232

Contents xiii8.2.48.38.48.5How do nucleoporins function inplant-microbe symbiosis?The nuclear pore and plant defence8.3.1 Plant immune responses can be triggered bypathogen-associated molecular patterns andmicrobial effectors8.3.2 AtNUP88 and AtNUP96 are required for basal andNB-LRR-mediated plant immunity8.3.3 Mechanisms of nucleoporin-mediated plantdefence signallingSpecificity, redundancy and general functions of plantnucleoporins8.4.1 The NUP107-160 sub-complex8.4.2 Hormone signalling8.4.3 Development, flowering time, stress tolerance andRNA transportChallenges and conclusionReferencesIndexColor plate (between pages 104 and 105)233235235236237239239242243245246255

LIST OF CONTRIBUTORSSusan J. ArmstrongSchool of BiosciencesUniversity of BirminghamB15 2TTUKAndreas BinderFaculty of Biology, Genetics, University of Munich (LMU)Großhaderner Straße 482152 MartinsriedGermanyJoanna BorucDepartment of Molecular GeneticsThe Ohio State UniversityColumbusOH 43210USAJohn A. BryantBiosciencesUniversity of ExeterExeterEX4 4QD, UKDavid E. EvansDepartment of Biological and Medical SciencesFaculty of Health and Life SciencesOxford Brookes UniversityHeadington CampusOxfordOX3 0BPUKF. Chris H. FranklinSchool of BiosciencesUniversity of BirminghamB15 2TTUKxv

xvi List of ContributorsMartin W. GoldbergDepartment of Biological and Biomedical SciencesUniversity of DurhamDurhamDH1 3LEUKKatja GraumannDepartment of Biological and Medical SciencesFaculty of Health and Life SciencesOxford Brookes UniversityHeadington CampusOxfordOX3 0BPUKIris MeierDepartment of Molecular GeneticsThe Ohio State UniversityColumbusOH 43210USAEugenio Sanchez-MoranSchool of BiosciencesUniversity of BirminghamB15 2TTUKKim OsmanSchool of BiosciencesUniversity of BirminghamB15 2TTUKMartin ParniskeFaculty of Biology, GeneticsUniversity of Munich (LMU)Großhaderner Straße 482152 MartinsriedGermany

List of Contributors xviiMonica PradilloDepartmento de GeneticaFacultad de BiologiaUniversidad ComplutenseMadrid28040 SpainNicola Y. RobertsSchool of BiosciencesUniversity of BirminghamB15 2TTUKJuan L. SantosDepartmento de GeneticaFacultad de BiologiaUniversidad ComplutenseMadrid28040 SpainChristophe TatoutGReD LaboratoryUMR CNRS 6293INSERM U1103University Blaise PascalAubièreFranceMélanie ThomasGReD LaboratoryUMR CNRS 6293INSERM U1103University Blaise PascalAubièreFranceEmmanuel VanrobaysGReD LaboratoryUMR CNRS 6293INSERM U1103University Blaise PascalAubièreFrance

xviii List of ContributorsJavier VarasDepartmento de GeneticaFacultad de BiologiaUniversidad ComplutenseMadrid28040 SpainXiao ZhouDepartment of Molecular GeneticsThe Ohio State UniversityColumbusOH 43210USA

PREFACEThis volume was conceived to bring together reviews describing recentadvances in knowledge and understanding of plant nuclear structures andfunctions, including that of the nuclear envelope. The book is particularlytimely in that recent progress has been rapid in key areas including description and characterization of proteins of the nuclear envelope and nuclearpore complex, novel insights into nucleoskeletal structures, as well as developments related to chromatin organization, function and gene expression.Together these advances provide a framework for comparative understanding of nuclear envelope structure and function in a range of organisms andfor understanding its evolution.Current knowledge of the dynamic structure of plant DNA and chromatinis discussed by Sanchez-Moran in Chapter 5. Despite intensive study ofhistones and other chromosome-associated proteins, interactions to achievethe complex structures required both in interphase and during cell divisionremain poorly understood. The structures require several levels of organization, the first being the nucleosomal fibre comprising DNA wrapped arounda core of histones. This is a dynamic structure and mechanisms for its remodelling are described. The nucleosomal fibre is then wound into a structuretermed the chromatin fibre, which is arranged in loops associated with amulti-protein chromosome scaffold, the third level of structure. This interphase structure undergoes rapid dynamic change in mitosis with furthercondensation for replication and division. The importance of the structuralorganization of chromatin for processes such as transcription, replication,repair, recombination, condensation and segregation is also discussed. As inmetazoans, plant chromatin is organized into regions of hetero- and euchromatin with heterochromatin adjacent to the NE.Recent advances in understanding heterochromatin structure are presentedin Chapter 6 by Vanrobays et al. Heterochromatin, originally thought tobe condensed, gene-poor and ‘silent’, is now known often to be preferentially localized to the nuclear envelope and nucleolus and its significanceis becoming clear as an epigenetic state required for many functions of thegenome, including gene regulation, segregation of chromosomes and maintaining stability of the genome. Despite limited knowledge of it, in mostspecies heterochromatin is the main form of chromatin and key questionsremain to be answered. How is spatial organization of heterochromatin maintained through the cell cycle as DNA is replicated, chromatin condensed, andthe nuclear envelope disrupted and reformed? Interactions between nuclearxix

xx Prefaceenvelope, nucleoskeleton and chromatin are likely to be very significant andare discussed together with other theories for heterochromatin positioning.Plant genomes vary greatly in size but in all cases the genome is contained within a very small compartment and it is clear that complex threedimensional organization is needed in order for the many processes requiredfor function. This three-dimensional structure requires interactions betweenchromatin, the envelope, the nuclear pores and the rest of the cell. In Chapter 4, Goldberg discusses from an ultrastructural and biochemical perspectivethe presence of an equivalent of the highly ordered lamina and nucleoskeletondescribed in metazoans. Such a structure appears to be required for nuclearfunction, but until recently its protein composition has eluded plant scientists.Plant cells have no proteins homologous to the lamins or other intermediatefilament protein. Recent electron microscope studies in Goldberg’s laboratoryof the inner face of the plant nuclear envelope reveal a filamentous structureinterconnecting the NPCs. This appears to be organized similarly to the lamina of Xenopus oocytes. Protein candidates for a plant nucleoskeleton haverecently been suggested from a number of approaches; these long coiled-coilnuclear-localized proteins show some similarities to nucleoskeletal proteinsof the metazoans and Goldberg presents the growing, but as yet incomplete,evidence for their role. The likely (direct or indirect) interactions of these proteins with the proteins of the nuclear envelope via a ‘Linker of Nucleoskeleton and Cytoskeleton’ complex is also considered in Chapter 2 by Graumannand Evans. Therein, the authors describe that, in common with metazoans,plants have one key family of proteins that in other kingdoms constitutesthe inner nuclear envelope component of this bridging complex, namely theSad1/Unc84 (SUN)-domain prot

Dr Jocelyn K.C. Rose, Department of Plant Biology, Cornell University, Ithaca, New York 14853, USA. Titles in the series: 1. Arabidopsis Edited by M. Anderson and J.A. Roberts 2. Biochemistry of Plant Secondary Metabolism Edited by M. Wink 3. Functions of Plant Secondary Metabolites and their Exploitation in Biotechnology Edited by M. Wink 4.

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