Membranes:Specialized Functionsin Plants

M. SmallwoodThe Plant Laboratory, Department of Biology, University of York, PO Box 373,York YO1 5YW, UK

J.P. KnoxCentre for Plant Biochemisty and Biotechnology, University of Leeds,Leeds LS2 9JT, UK

D.J. BowlesThe Plant Laboratory, Department of Biology, University of York, PO Box 373,YorkYOl 5YW, UK

tos'SCIENTIFICPUBLISHERS

Contents

ContributorsAbbreviationsPreface

Membranes and the Cell Surface

1. Interactions between the plasma membrane and the cytoskeleton in plants.C.W. LLoyd, B.K. Dr0bak, S.K. Dove and C.J. Staiger 1Introduction 1

The cortical cytoskeleton is dynamic 1Microtubule/plasma membrane interactions 2

The wall influences MT stability and alignment 2Calcium and phosphorylation as modulators of MT behaviour 4Microtubule-associated proteins (MAPs) 5Other components of the cortical cytoskeleton 5

Microfilaments 6Microfilament/plasma membrane interactions 6Control of actin organization: actin-binding proteins (ABPs) 8Control of actin organization: polyphosphoinositides 11Control of actin organization: calcium-dependent protein kinase (CDPK) 13GTP-binding proteins and cytoskeletal dynamics 13

Prospects 14References 15

2. Cell adhesion in plants and its role in pollination. EM. Lord, L.L. WallingandG.Y.Jauh 21

'if- .,,I^i21

.,,I^idenjp€^pi£3fd!j^ion\iolecules in pollination 26' d e l i l ^ n g t th a i i l e h i o t i in l a t ll: mthere a similar mechanism operating in plant cell

y j ^ p ^ l l y in tip-growing cells? 29;i A"ctin-6ased mo^fy models for animal cells 29

'pyMiimtiffliracase of cell movement in plants? 30During growth, are plant cells attaching to and spreading on their ECMs? 33

References 34

3. Membrane conservation during plasmolysis. K.J. Oparka, DAM. Priorand J.W.Crawford 39Introduction 39Alterations of the plasma membrane (PM) during plasmolysis 39Hechtian strands 40Hechtian attachment sites 40Wall-membrane interactions during plasmolysis 41

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Hechtian strands arise during freezing of cold-hardened plant cells 43PM vesiculation 44Deletion of the tonoplast during plasmolysis 45PM vesiculation during freezing 45Hechtian strands versus PM vesicles 46PM-endoplasmic reticulum (ER) interactions during plasmolysis 47The cytoskeleton during plasmolysis 48Plasmodesmata 50Structure of plasmodesmata following plasmolysis 50Retention of desmotubules 51ER-plasmodesmata interactions 52A structural model of the plasmolysed plant cell 53References 53

4. Cellulose biogenesis. R.L. Blanton and C.H. Haigler 57Introduction 57The plasma membrane specializations associated with cellulose synthesis 57Biochemistry of cellulose polymerization in higher plants 61Non-plant models for cellulose synthesis 64

Bacterial cellulose synthesis 64Protistan cellulose synthesis 66

New approaches to plant cellulose biogenesis 67UDP-Glc photoaffinity probes 67Cellulose synthesis inhibitors 68Genetic approaches to cellulose synthesis 68Sequence analysis 69Related proteins 69

Concluding remarks 69References 70

5. Callose synthesis. H. Kauss 11Occurrence and functions of callose 77Callose in higher plants 77

Developmentally regulated callose deposition 77Callose induced by stress 78

Callose in lower plants 79Chemical nature of callose 80Which membranes synthesize callose? 81Properties of p-glucan synthases in vitro 81

(3-Glucan synthase I (GS I) 81(3-Glucan synthase II (GS II, callose synthase) 82

Induction of callose synthesis in vivo 85Some unanswered questions 88References 89

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6. Arabinogalactan-proteins: developmentally regulated proteoglycansof the plant cell surface. J.P Knox 93Introduction 93AGP structure 93AGPs and the plasma membrane 94AGP localization: the impact of hybridoma technology 95

Developmental dynamics of AGP epitopes 95AGPs: metabolism and interactions 97AGPs: possible functions and prospects 98References 100

7. Signal perception at the plasma membrane: binding proteins and receptors.M.G. Hahn 103Introduction 103Hormone-binding proteins 104

Auxin-binding proteins 104Abscisic acid-binding proteins 109Gibberellin-binding proteins 110

Oligosaccharin-binding proteins 111Hepta-P-glucoside elicitor-binding proteins 113Oligochitin elicitor-binding proteins 114Glycopeptide elicitor-binding proteins 116Oligogalacturonide-binding proteins 117

(Poly)peptide elicitor-binding proteins 118P. sojae peptide elicitor-binding proteins 118Elicitin-binding proteins 119

Fusicoccin-binding proteins 120Conclusions 124References 126

8. Plant membrane-associated protein kinases: proposed great communicators.A.C. Harmon, J.-Y. Lee, B.-C. Yoo and J. Shao 137Introduction 137Receptor protein kinases 137

Animal receptor protein kinases 137Plant receptor-like protein kinases 138

The putative blue-light receptor 141Other membrance-associated protein kinases 142

Membrane-associated calmodulin-like domain protein kinase 142Light-harvesting complex II kinase 144

ETR1: a plant homolog of a prokaryotic two-component system? 145Conclusions 146References 146

9. A role for the heterotrimeric G-protein switch in higher plants. K. Palme 151Introduction 151GTPases switch between inactive and active states 151Heterotrimeric G proteins 153

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Ga genes 154GP genes 155G-protein-coupled receptors 155Target proteins 157Gp-like proteins 158Perspectives 159References 159

Membrane Lipid Metabolism

10. Lipid transfer proteins: structure, function and gene expression.J.-C. Kader, M. Grosbois, F. Guerbette, A. Jolliot and A Oursel 165Introduction 165Assay and purification of LTPs 166

Assay 166Purification 167

Biochemical properties of LTPs 167Molecular mass 167Isoelectric point 168Specificity 168

Structure and mode of action of LTPs 168Amino-acid sequence 168Structural model 168Mode of action 169

Cell localization and biogenesis 170Biogenesis 170Cell localization 171

Gene expression 171Isolation of cDNAs and genomic clones 171Gene expression 172

Physiological roles 172Intracellular roles 173Extra- or intercellular roles of LTPs 174

Conclusions 175References 175

11. Plant galactolipids and sulfolipid: structure, distribution and biosynthesis.J. Joyard, E. Marechal, M.A. Block and R. DouceIntroductionStructure, distribution and properties of plastid glycolipids

Structure and distribution of galactolipids and sulfolipidPhysical properties of plant glycolipids

Biosynthesis of chloroplast glycerolipidsOrigin of the diacylglycerol backboneGlycolipid biosynthesisFatty acid desaturation

ConclusionsReferences

Contents ix

12. Metabolism of plant phosphoinositides and other inositol-containing lipids.B.K. Dr0bak 195Inositol-containing lipids in plants 195The plant phosphoinositide system 197Biosynthesis and turnover of plant phosphoinositides 198

Phosphatidylinositol 198Phosphatidylinositol 4-phosphate (PtdIns(4)P) and phosphatidylinositol

4,5-bisphosphate 199Turnover of 4-phosphorylated plant phosphoinositides 199Phosphoinositide kinases 199Polyphosphoinositide phosphatases 200Phospholipase C and other other phospholipases 201Phospholipases A and D 201

3-Phosphorylated phosphoinositides 202Regulation of phosphoinositide turnover 203

Formation of signalling complexes: signal-responsive, and unresponsivephosphoinositide pools 203

Activation of mammalian and plant PLC isoforms 204Plant phospholipase C (type II) 205Interactions between the phosphoinositide pathway and components

of the cytoskeleton 206Glycophosphosphingolipids and other complex inositol-containing lipids 208Conclusions and future research 208Notes added in proof — update 209

Phospholipase C 209Ins(l,4,5)P3 production 209Phosphatidylinositol 3-kinases 210Novel phosphoinositides 210Tyrosine kinases 210Cytosolic Ca2+-fluxes 210

References 210

13. Jasmonates: global regulators of plant gene expression. G.J. Loake 215Role of membranes in cell signalling 215Jasmonates as global regulators of gene expression 215Jasmonate biosynthesis 216Jasmonate-induced developmental responses 218Jasmonate-induced genes and proteins 219Modulation of jasmonate signals 220Genetic dissection of the jasmonate-signalling pathway 221Role of jasmonates in wound signalling 222Role of jasmonates in disease resistance 225Methyl jasmonate: an airborne interplant signal 226Transcriptional activation by jasmonates 226Summary 227References 228

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Regulation of Membrane Permeability

14. Functions of ion channels in plant cells. M. Tester 231Introduction 231What are ion channels? 231Measurement of ion channels 232Primary structure of ion channels 233Properties of ion channels 234

Mechanism of ion movement: conduction 234Selectivity of ion movement 234Control of ion movement: gating 235Pharmacology of ion channels 235

Classification of ion channels 236Roles of ion channels in plants 236

Role of ion channels in nutrient uptake 236Role of ion channels in intracellular malate movements 238Role of ion channels in movements of guard cells 238Role of ion channels in movements of other plant parts 238Role of ion channels in long-distance signalling within plants: systemic

wound responses 239Role of ion channels in signal transduction and control of development 239Role of ion channels in charge balance 240

Conclusions 241References 241

15. Mechanosensitive ion channels. A. Garrill, G.P. Findlay andS.D. Tyerman 247Introduction 247Studying MS channels 247MS channel genes 248Channel gating 249Clustering of channels 251Pharmacology 251MS channels in walled cells 251

Higher plant cells 251Fungi 253Bacteria 254

Functions 254Osmoregulation 254Tropic responses 255Generation of Ca2+ gradient in polarized growth 256Cell cycle regulation 256

Channel evolution 256Non-channel MS proteins 257Future work 257References 257

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16. Proton-translocating ATPases of the plasma membrane: biologicalfunctions, biochemistry and molecular genetics. B. Michelet andM. Boutry 261Introduction 261

General aspects of transport and ATPases 261Demonstration of the existence of the plasma-membrane H+-ATPase 262

Biochemistry and molecular biology 263Properties of the enzyme 263Structure and function 263Activity modulation: auxin, fusicoccin, light, phospholipids and kinases 265Gene regulation and tissue-specific expression 266Modification of H+-ATPase expression 267

Physiological functions of H+-ATPase 267A housekeeping enzyme? 267Mineral nutrition 268Transport of organic molecules 270Salinity tolerance and turgor regulation 271Intracellular pH regulation 272Acid growth 272Other less well-documented functions 273

Conclusions 274References 274

17. Calcium efflux transporters in higher plants. P. Askerlund andM. Sommarin 281Introduction 281Plasma membrane 282Endoplasmic reticulum 286Vacuole membrane 287Mitochondria and plastids 288Purification and cloning of Ca2+ transporters 289Regulation of Ca2+-ATPases 291Concluding remarks 294References 295

18. Electrical signalling in plants. J.F. Thain andD.C. Wildon 301Introduction 301The characteristics of electrical signals 301Experimental methods 302Electrical signalling in plants: cases and candidates 303

Leaf movements 303Respiration and photosynthesis 303Transport of assimilates and phloem unloading 303Plant development 304Protein synthesis 304

Mechanism: the nature of the signal 304Possible mechanisms 304Action potentials in plants: evidence obtained with intracellular

microelectrodes ' 304

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Propagating action potentials in plants: evidence obtained with surface-contact electrodes 306

Individual cases 307Pathways for electrical signalling 309

Pathways for short distances 309Pathways for longer distances 310Excitable cells of the vascular pathway 310Propagation of excitation in plant tissues 312Propagation of excitation in the whole plant 312

Initiation and transduction of electrical signals 313Signal initiation 313Signal transduction 313

Conclusions 314References 315

19. Sugar transport in higher plants. W.B. Frommer, B. Hirner, C. Kiihn,K. Harms, T. Martin, J.W. Riesmeier and B. Schulz 319Introduction 319Plastidic sugar transport 319Plasma membrane sugar transport 321

Symplastic transport 321Apoplastic transport 322Other proteins involved in phloem loading 325Regulation of phloem loading 327A hypothetical model for phloem loading 327Phloem unloading 328

Conclusions 330References 330

Membrane Compartments within the Cell

20. The Golgi apparatus and pathways of vesicle trafficking. C. Howes,L. Faye and B. Satiat-Jeunemaitre 337Introduction — the pathways of vesicle traffic in plant cells 337Budding, targeting and fusion of vesicles 338

Vesicle budding and coats 339Vesicle uncoating and targeting 340Vesicle fusion 341Small GTP-binding proteins may regulate vesicle trafficking 341

Driving forces for vesicle transport 342Through the Golgi stack 343

Golgi structure 343Enzyme distribution, function and retention within the Golgi 345Transfer down the Golgi stack — cisternal maturation or vesicle shuttles? 349

Transport to and from the Golgi apparatus 350ER/Golgi communication 350Golgi-vacuole pathways 352Golgi-cell surface transport 352

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Bypassing the Golgi 354Endocytosis — the way in 354

Mapping the pathway 354Do smooth endocytic vesicles help to balance the membrane economy

of the cell? 356Receptor-mediated endocytosis 356

Conclusions and prospects 357References 357

21. Mechanisms controlling function, identity and integrity of the plantendoplasmic reticulum. /. Denecke 367Introduction 367Polypeptide synthesis and translocation, a multi-step process 368

The targeting of mRNA to the ER membrane 368Requirement for chaperones on either side of the membrane 369Protein modification during translocation 369

ER proteins and their role in protein biosynthesis and folding 370The lumenal binding protein (BiP), a lumenal Hsp70 homologue 371Endoplasmin, the lumenal Hsp90 homologue 371Protein disulphide isomerase (PDI) 372Calreticulin and calnexin 372Novel components of the ER lumen and membrane with a suggested

chaperone function 373Autoregulatory mechanisms to guarantee ER integrity 373

How do ER-resident proteins accumulate in the ER? 373How is the nucleus informed about the need for more chaperones? 375

External control of ER activity 377Future prospects 378References 378

22. Endoplasmic reticulum in the cortex of plant cells. I.K. Lichtscheidland P.K. Hepler 383Introduction 383Role of cortical cytoplasm 383Organization of cortical ER in mature plant cells 384ER dynamics and corresponding organelle movement 387Physiological properties of the cortical ER 390ER and the formation of the cell plate and cell wall 393

Formation of the cell plate during cytokinesis 393Deposition of local wall thickenings 393Expansion and development of primary walls 394

Intracellular communication via plasmodesmata 395Role of cortical ER in response to endosymbionts and parasites 395Conclusions 396References 397

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23. Targeting and trafficking of vacuolar proteins. T.L ReynoldsandN.V. Raikhel 403Introduction 403Secretory system 403Soluble protein sorting to the vacuole 404

C('s-acting factors 404Trans-acting factors 408

Vacuolar membrane (tonoplast) protein sorting 409Plants 409Mammalian and yeast systems 410

Components of the vacuolar sorting machinery 411vps mutants 412Small GTP-binding proteins 413

Conclusions 414References 415

24. Biogenesis of plant peroxisomes. A. Baker 421Introduction 421Ontogeny and development 422

Germination 422Greening 422The glyoxysome-peroxisome transition 423Senescence 424

Peroxisomal protein targeting 424Carboxyl-terminal signals 425Amino-terminal signals 426Internal signals 426Isocitrate lyase 427Membrane proteins 427

Membrane lipids 428Import mechanisms 428

Energy requirement 428Protein conformation during import 429Protein assembly 430Receptors 430

Unanswered questions 431Import mechanisms 431Evolutionary origins 431Growth and division of peroxisomes 431

References 435

25. Biogenesis of chloroplasts in higher plants. J.C. Gray 441Introduction 441Chloroplast development and division 442

Plastid differentiation 442Chloroplast number and size 442Chloroplast DNA replication and distribution 443

The role of the plastid genome in chloroplast biogenesis 444The role of the nuclear genome in chloroplast biogenesis 446

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Nuclear genes encoding chloroplast proteins 446Nuclear genes regulating chloroplast development 448

Co-ordination of chloroplast and nuclear gene expression 449Chloroplast control of nuclear gene expression 449The 'plastidic factor' 450

The role of mitochondria in chloroplast biogenesis 452Conclusions 452References 453

26. Translocation of proteins across chloroplast membranes. C. Robinson 459Introduction 459Translocation of proteins into and across the envelope membranes 459

Early steps in the import process 459Translocation of proteins across the envelope membranes 460Events in the stroma 462A different import mechanism for outer envelope membrane proteins 463

Integration of proteins into the thylakoid membrane 463The biogenesis of nuclear-encoded thylakoid lumen proteins 464

A general two-stage import pathway for thylakoid lumen proteins . 464Two distinct mechanisms for the translocation of proteins across the

thylakoid membrane 464The possible origins of parallel translocation pathways for lumenal proteins 465

Concluding remarks 466References 467

Plasmodesmata

27. Plasmodesmatal networks in apical meristems and mature structures:geometric evidence for both primary and secondary formationof plasmodesmata. T.J. Cooke, M.S. Tilney and L.G. Tilney 471Introduction 471The definition of primary and secondary plasmodesmata 471

Structural approach 472Developmental approach 472Geometric approach 473

Plasmodesmatal networks in lower vascular plants 473General aspects of apical meristem construction in ferns 473Plasmodesmatal densities in fern apical meristems 476Plasmodesmatal densities in mature structures of ferns 476Conclusions 478

Plasmodesmatal networks in angiosperms 479General aspects of apical meristem construction in angiosperms 479Plasmodesmatal densities in angiosperm apical meristems 481Plasmodesmatal densities in mature structures of angiosperms 483Conclusions 484

Discussion 485General features of plasmodesmatal networks 485Evolutionary consequences of plasmodesmatal networks 485

References 486

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28. Secondary plasmodesmata: biogenesis, special functions and evolution.B. Ding and W.J. Lucas 489Introduction 489Biogenesis and structure of higher plant secondary plasmodesmata 491

Mechanisms of biogenesis 491Regulation 496Structure 496

Special functions of higher plant secondary plasmodesmata 497Co-ordination of growth and development 498Interactions with viral infection 502

Evolutionary aspects of secondary plasmodesmata 502Future prospects 503References 503

Modified Membranes in Symbiotic Relationships

29. Plant membrane structure and function in the Rhizobium-legumesymbiosis. N.J. Brewin 507Endosymbiosis and biological nitrogen fixation 507Peribacteroid membrane: the symbiotic interface 508

Components of the peribacteroid membrane 510Properties of the peribacteroid membrane 513

Plasma membrane 516Tissue and cell invasion by Rhizobium 516Signal transduction in nodule initiation 518

Conclusions 519References 520

30. Membranes in mycorrhizal interfaces: specialized functions in symbiosis.S.E. Smith and F.A. Smith 525Introduction 525Membranes in the interfaces of mycorrhizal associations 525

Types of interface 525Plasma membranes of plant and fungus 528The apoplast 531Intracellular membranes 531

Transport processes 532Extramatrical mycelium and phosphate uptake from soil 532Transport at the interface 533

Recognition and colonization: speculation about the involvement of plasmamembrane receptors 535

Summary and conclusions 538References 538

31. The plant plasma membrane in fungal disease. J.A. Callow andJ.R. GreenIntroductionConsequences of disease for specific membrane functions

The H+-ATPase

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Specific carriers and ion channels 545Cell wall synthesis and repair 546Redox functions 546Recognition and transduction of pathogen signals 547Vesicle transport across plasma membranes 550

Hypersensitive resistance: the role of substrates provided by the lipid bilayer 550Structure, function and assembly of modified plasma membranes associated

with haustoria 551Structure and composition of the EHM 553Development and application of monoclonal antibody probes to explore

molecular differentiation in the EHM 554Localization of ATPase activity and the role of neckbands 554Role of the invaginated plasma membrane in transport of solutes 556Assembly of the EHM 557

References 558

Index 563