Stomata

Stotnata SECOND EDITION

Colin Willmer University of Stirling, UK

and

Mark Fricker University of Oxford, UK

I~nl SPRINGER-SCIENCE+BUSINESS MEDIA, B.v.

Flr,t cdltlon 1983

Selond edltIon 1996

© 1996 Cohn WIllmcr and Mark Fnlkcr Originally published by Chapman and Hali in 1996 Sot\cover reprint of the hardcover 2nd edition 1996

Type,et m Garamond 10 5/12pt bv Saxon Graphll' Ltel, Derbv

Pnnted m Great Bntam lw St Felmunchbur\ Pre" Bul)' St Edmund" Suffolk

ISBN 978-94-010-4256-7 ISBN 978-94-011-0579-8 (eBook) DOI 10.1007/978-94-011-0579-8

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Contents

Preface to the second edition ix

Preface to the first edition xi

Acknowledgements xiii

1 Introduction 1 1.1 General considerations about stomata 1 1.2 Historical aspects 2 1.3 The importance of research into stomatal functioning and

behaviour 7 References 8

2 The distribution of stomata 12 2.1 Location and occurrence of stomata 12 2.2 Stomatal frequency 17 2.3 Stomatal patterning 24 2.4 Heterogeneity in stomatal characteristics and responses 26

References 30

3 The structure and development of stomata 36 3.1 Anatomy and morphology of the leaf epidermis 36 3.2 Development and differentiation of stomata 49 3.3 The ultrastructure of guard cells 64

References 82

4 The mechanics of stomatal movements 92 4.1 Introduction 92 4.2 Water relations of guard cells 92 4.3 The physico-chemical aspects of stomatal movements 96 4.4 Morphological changes of the plasma membrane and

tonoplast of guard cells during stomatal movements 103 4.5 PhYSiological and mechanical properties of GCPs 104

References 106

5 The theory of gas diffusion through stomata 110 5.1 Introduction 110 5.2 Fick's law and the driving forces for diffusion 110 5.3 The analogy between electrical circuits and leaf resistances 113 5.4 Diffusion through a Single pore and multipores 115

VI CONTENTS

5.5 Cuticular conductance 120 5.6 Boundary layer conductance 121 5.7 Water use efficiency 123

References 124

6 Stomatal responses to environmental factors 126 6.1 Introduction 126 6.2 Interaction of environmental factors which influence stomatal

behaviour 126 6.3 Stomatal responses to light quality and quantity 131 6.4 Carbon dioxide 144 6.5 Temperature 148 6.6 Plant water status and atmospheric humidity 152 6.7 Mineral nutrition 161 6.8 Circadian rhythms and shorter-term oscillations in stomatal

movements 161 6.9 Stomatal activity during the life cycle of a leaf 165 6.10 Stomatal behaviour in canopies 168 6.11 Gaseous environmental pollutants and stomata 169 6.12 Plant pathogens and stomata 172

References 177

7 The influence of hormones and other naturally occurring compounds on stomatal behaviour 192

7.1 Introduction 192 7.2 Abscisic acid 193 7.3 Other sesquiterpenoids (xanthoxin, all-trans farnesol,

vomifoliol, phaseic acid) 208 7.4 Other hormones 209 7.5 Fatty acids 212 7.6 Phytotoxins 212 7.7 Phytoalexins 215 7.8 Other compounds 215 7.9 Artificial control of stomata 216

References 218

8 Ionic relations of stomatal movement and signal transduction in guard cells 228

8.1 Introduction 228 8.2 The involvement of ions in stomatal movements 228 8.3 Ion fluxes and the driving forces for ion movement 244 8.4 Summary of ion movement events during stomatal

movements 267 8.5 Signal perception and transduction by guard cells 267

References 293

CONTENTS VII

9 The metabolism of guard cells 310 9.1 Introduction 310 9.2 The flow of carbon from starch to malate during stomatal

opening 315 9.3 The fate of malate during stomatal closure 330 9.4 The role of chloroplasts in guard cells 335 9.5 Metabolite transport into guard cells and sucrose

metabolism 339 9.6 The energy relations of stomatal movements 341 9.7 Lipid metabolism in guard cells 344

References 345

10 Recent developments and future research 354 10.1 Introduction 354 10.2 Stomatal distribution and patterning 354 10.3 Cell and tissue differentiation 355 10.4 Mechanical relations of the epidermis 356 10.5 Diffusion of gases and the role of stomata 356 10.6 Environmental effects 356 10.7 Hormone action 358 10.8 Ion transport and signalling 360 10.9 Intermediary metabolism and its regulation 360 10.10 Molecular biology of stomata 361

References 364

Index 367

Preface to the second edition

In 1902 Copeland published a paper (B.E. Copeland, Ann Bot., 16, 327-364, 1902) in which he stated:

The movements of stomata have been familiar to botanists for more than a century. From all points of view, anatomical and physiological, the stomata have received more constant and lasting attention probably than any other single vegetative structure in the plant. And yet recent lit­erature on the subject is most contradictory, not only as to the mecha­nism of their movements, but even as to the conditions which influence their opening and closing.

Essentially these same sentiments can still be applied nearly a century later. Stomata continue to be a source of intense research endeavour and the results of the research often appear contradictory; debate and controversy about various aspects of their function and functioning con­tinues. True, over the last few decades major advances in our under­standing of the behaviour of stomata and how stomata function have been made, but much still remains to be discovered. Nevertheless, now seems an appropriate time to update what has been added to our knowledge since the first edition of Stomata was published in 1983. Because the subject has become much more complex and encompasses a wide array of topics, including cell anatomy and ultrastructure, physi­ology, ecology, intermediary metabolism, ion relations and molecular biology, this second edition has expanded significantly and two authors were deemed necessary to do justice to the subject. Thus Mark Fricker co-authors this second edition with Colin Willmer.

Although the basic framework of the first edition exists in the second edition, virtually the whole text has been rewritten. A new chapter has been added on the theory of gas diffusion through stomata; sections on ionic relations of guard cells and on signal perception and transduction by guard cells have been expanded greatly to reflect the recent progress in these areas; and a section on the genetics and molecular biology of guard cells has been inserted in a concluding chapter.

Colin Willmer University of Stirling

Mark Fricker University of Oxford

November, 1994

Preface to the flrst edition

Over the last decade enormous advances 10 our understandmg of the functionmg of "tomata have been made Today, the overall pattern of events 10 stomatal functloOlng IS generally under~tood although some of the fmer details of the mechaOlsm remam to be eluCIdated However, the mechaOlsm whereby changmg CO2 levels wlthm a leaf control stom­atal movements remam~ one of the biggest puzzles

The excellent text PhYSlOlogy of Stomata, by Professors H Meldner and T A Mamfleld, I~ over 12 years old and mevltably sections of It are now outdated Although numerou~ flOe review,> on vanous aspects of stomata have been wntten 10 the meantime, none could be conSidered as complete, compact appraisals of the subject dnd thus to have super­seded the Meldner and Mansfield book Now IS therefore an appropnate time to review the statu~ of our knowledge about stomata

This book encompas~es all a~pect~ of the subject except the phySICal processes mvolved 10 the exchange of gases between a leaf and ItS envI­ronment ThiS topIC IS dealt With very adequately 10 a vanety of other books and reVlew~, and the subject matter, With mmor differences of opmlon, remams much the '>ame today as It was perhaps 20 years ago A descnption of how to measure stomatal apertures and the use of porometers has been restncted to a fmal chapter whICh also deals with expenments which can be carned out by students Agam, there are numerous text~ and paper~ whICh deal 10 greater detail With the theory and use of porometers than that descnbed here

In a text of thiS type, which IS not mtended to be a research treatise but a more general, though detailed appraisal of the subject mtended for undergraduate and postgraduate students '>peClahzmg 10 plant SCI­ences, references must be hmlted

Choosmg the limited number of references was difficult I have tend­ed to quote the more recent references, Important and major artICles of the past, and review artICles Inevitably, however, some statements remam unsupported by a reference Also, 10 attempts to keep the book a~ current as po~slble, I have drawn on mformation from a number of unpublished works

Where contentious Issues anse I have attempted to state each view but space has not always allowed me to diSCUSS the detailed eVidence supportmg each view The reader, 10 some cases, IS left to read the ongl­nal reports to deCIde the most convmcmg lme of argument

XII PREFACE TO THE FIRST EDITION

I have also tried to be specific about the plant species used in a partic­ular experiment because, although there are certain basic features and processes concerning stomatal functioning and behaviour which are common to all species, there may well be variations on this common theme depending on the species.

Colin M. Willmer University of Stirling

1982

Acknowledgements

Authors' acknowledgements, second edition

We would like to thank the followmg people who have reviewed parts of our manu~cnpt or who have advI~ed us and/or supplied u~ wlth unpub­lished mformatlon Peter Ayre.." Umverslty of Lancaster, MlChael Blatt, Wye College, Umverslty of London, Dudley Bowlmg, Umverslty of Aberdeen, Judy Croxdale, Umver..,lty of Wlsconsm, Bill Davies, Umverslty of Lancaster, Peter Dmnch, Umver~lty of Mumch, Alistair Hethenngton, Umverslty of Lanca~ter, Nick Kruger, Umverslty of Oxford, Jane Langdale, UmveNty of Oxford, Gerard Lasceve, CEN, Cadarache, Terry Mansfield, FRS, Umver'ilty of Lanca~ter, Hans Meldner, Umverslty of Stlrlmg, Hugh Nimmo, UnlveNty of Glasgow, Bill Outlaw, Umverslty of Flonda State, Tallaha~see, Robm Phillips, Umverslty of Stlrlmg, Klau~ Raschke, Umver..,lty of Gottmgen, Robert Scotland, Umverslty of Oxford, Ken-lChlro Shlmazaki, Kyushu Umverslty, Fukuoka, Japan, Andrew Smlth, Umver..,lty of Oxford, Jonathan Weyers, Umverslty of Dundee, Alam Vavas~eur, CEN, Cadarache, Eduardo Zeiger, University of Califorma, Lo~ Angeles

We would like to empha~lze that any errors, mlsmformatlon or faulty rea~onmg whICh remam 10 the book are solely our responslblhty

Author's acknowledgements, first edition

I am partlCularly mdebted to Professor 0 A Baker, who edlted my man­uscnpt and gave valuable advice A speCial thanks goes to Professors J E Varner and H Meldner, both of whom read much of my manuscnpt and a number of Improvements resulted from their cntlClsms

Thanks are also due to the followmg Dr W H Outlaw Jr of the Department of Biological SCiences, Flonda State Umverslty, Tallahassee, Drs P Brown, J Mamotls, Barbara Pickard and others wlthm the Department of Biology, Washmgton University, St LOUIS, all of whom helped me m their mdlVldual way~, colleagues wlthm the Department of Biology, Umverslty of Stlrlmg, for their comments and oplmons about vanous pomts, T Forrest, W Struthers and L Taylor of the Department of Biology, Umverslty of Stlrlmg for EM and photographic work, numer-

XN ACKNOWLEDGEMENTS

ous people, whose names are mentioned 10 the figure or table legends, who gave me permission to use their published and unpublished data I also thank the followmg bodies who gave me permission to reproduce some of their published matenal the Amencan SOCiety of Plant Physiology, Spnnger-Verlag, Cambndge University Press, Blackwell SCientific Publications Ltd, the Institute of Biology, London, and the National Research CounCil of Canada

However, I am completely responsible for the views expressed 10 this book, for the pre~entatlon of ItS contents and any errors that may be found therem

I would also like to acknowledge that thiS book would not have been wntten Without the mfluence of Professor T A Mansfield, who, 10 the very begmnmg, gave me the opportUnity to study and research mto stomata and who mltlated my mterest 10 the subject

Publisher's acknowledgements, second edition

We are mdebted to the followmg for permission to reproduce copynght matenal AcademIC Press Ltd and the authors for our Fig" 6 2 and 6 11 from Figs 11 and 4 (WIll mer, 1988) and our Table 5 1 and Fig 8 5 from Table 81 and Fig 85 (Nobel, 1991), The Amencan SOCiety of Plant PhYSiologists for our Fig 8 10 from Fig 3 (Allan et al , 1994), our Figs 5 6 and 57 from Fig 9 (Tmg and LoomiS, 1965), our Figs 65 and 69 from Figs 4 and 5 (H~lao et al , 1973), our Fig 613 from Fig 1 (Cockburn et al, 1979), our Fig 92 (Gotow et al, 1985), our Fig 6 18a from Fig 2 (RadIO, 1984), our Fig 8B 2 from Figs 2 and 3 (Hednch and Schroeder, 1989) and our FIg 6 18b from Figs 1 and 2 (RadIO et al, 1982) all © Amencan SOCiety of Plant PhYSiologists, The Australzan Journal of Plant Physzology for our Fig 6 20 from Fig 3 (Constable and Rawson, 1980), The Botanzcal Journal of Scotland for our Fig 3 9 from Fig 4 (Willmer, 1993), The AmerzcanJournal of Botany for our Fig 55 from Fig 2 (Tmg and LoomiS, 1963) and our Fig 3 12 from Figs 2, 3, 5 and 6 (Sack and Paolillo, 1983), Cambndge University Press for our Fig 615 from Fig 2 (DaVies et al , 1981) and our Figs 63 and 66 from Figs 54 and 52 Oones, 1992), The Company of Biologists Ltd for our Fig 313 from Fig 31 (Galatls et al, 1986) and for our Fig 3B 1 from Fig 2 (Sholton, 1989), both 10 the Journal of Cell SClence, The Institute of Biology for our Fig 6 17 from Fig 10 (Mansfield, 1971), The Japanese SOCiety of Plant PhYSiologists for our Tables 9 4 and 9 5 from Tables 3 and 4 (Sato, 1985), Kluwer AcademIC Publishers for our Fig 6 7 from Fig 11 2 (Leshem and Will mer, 1992) and for our Fig 5 9 from Fig 1 (WIgley and Clark, 1974), Longman Group Ltd for our Figs 44 and 58

ACKNOWI EDGEMENTS xv

and Table 4 1 from Figs 2 4b, 3 5 and Table 2 2 (Methods zn Stomatal Research, Weyers and Meldner, 1990), Macmillan MagazInes Ltd and the authors for our Figures 2 4a and b from Figs 1 and 2 (Woodward, 1982), our Fig 8 12 from Fig 2 (Gilroy et al , 1990) and our Fig 89 from Fig 3 (McAmsh et aI, 1990), all from Nature, The National Academy of SCience, USA for our Fig 8 17 from Fig 5 (Thiel et ai, 1993), The National Research CounCil of Canada for our Fig 3 15 from Fig 2 (Allaway and Setterfield, 1972), our Fig 36d from Fig 30 (Dayanadan and Kaufman, 1973) and our Fig 77 from Fig 3 (Allaway and Mansfield, 1970) (all from the Canadzan Journal of Botany), New Phytologzst for our Fig 23 from Fig 2 (Miranda et at , 1981), our Fig 619 from Figs Ib and 2b (MartIn and Meldner, 1971), our Fig 79 from Fig 2 (Plumbe and Willmer, 1986) and our Fig 88 from Fig 4 (De Sliva et al , 1985), Oxford University Pres'> for our Fig 6 1 from Fig 2 (Heath and Russell, 1954), our Fig 64 from Fig 2 (TravI'> and Mansfield, 1984), our Fig 66 from Figure lA (Pemada'>a, 1982), our Fig 621 from Fig 3B (Willmer et al , 1988), our Fig 82 from Figs 2 and 3 (BowlIng, 1987) and our Fig 41 from Fig 2 (Edward,> and Meldner, 1979), all from the Journal of Experzmental BlOlogy, PhyslOlogza Plantarum for our Fig 6 10 from Fig 2 (FitZSimons and Weyer~, 1986), Blackwell SCience Ltd for our Fig 26 (Smith et aI, 1989), our Flg~ 3 16 and 36(e) from Figs 5C and lC (Rutter and Willmer, 1979) and our Fig 6 12 from Fig la (Monson and JarviS, 1983), all from Plant Cell and Enmronment, Spnnger-Verlag and the authors for our Fig 4 6 from Raschke (1979) Movements USIng Turgor MechaOisms, PhyslOlogy of Movements (eds W Haupt and ME Feilelb), 4, Fig 6a-e, our Fig 616 from Tenhunen et al (1980), Oecologza, 47, 365-367, Fig 2, our Fig 3 10 from Marc et at (1989), Planta, 179, 516-529, Fig 19a-c, our Fig 71 from Wnght (1977), Planta, 134, 183-189, Fig 5, our Fig 82 from Penny and BowlIng (1974), Planta, 119, 17-25, Fig" 2-5, Penny and BowlIng (1975), Planta, 122,209-212, Fig,> 1 and 2 and Penny et at (1976), Planta, 130, 291, Flg~ 1 and 2, our Fig 73 from Willmer et al (1978), Planta, 139, 281-287, Fig 4, our Fig 3 11 from Cleary and Hardman (1989), Protoplasma, 149, 76-81, Fig 40, our Fig 3 19a-e from Willmer and Sexton (1979), Protoplasma, 100, 113-124, Figs 1, 3, 5, 6 and 7 and our Fig 49 from Weyers and Fltz~lmons (1985), The PhyslOloglcat Propertzes of Plant Protoplasts (ed PlIet), p 158, Fig 4 In addition, we are also Indebted to

Longman Group Ltd for permb~lon to reproduce matenal from the fIr~t edition of thl'> book

XVI ACK.I\IOWJ.EDGEMENTS

Special acknowledgement

Advances in research are often due to an international exchange of ideas, and each generation of scientists pushes the frontiers of knowl­edge further forward. It is upon this foundation that the success of future generations of scientists depends. Perhaps nowhere is this more evident than in the field of stomatal physiology.

Additionally, throughout the ages, it is often the case that certain sci­entists working in a particular field stand out and their names remain indelibly associated with the subject of their endeavours. Three such names associated with research into stomatal behaviour and function­ing, all currently Professors Emeriti, are 'Peter' Heath, Hans Meidner and Klaus Raschke. We would like to acknowledge their life-long fascina­tion with the workings of stomata, their major contribution to our knowledge of the subject and the inspiration they have given to our­selves and others to continue the quest for a fuller understanding of stomata and their impact on the growth of plants.