Mohan L.R. Kaul

Male Sterility in Higher Plants

With 140 Figures and 205 Tables

Springer -VerJag Berlin Hei&lberg New York London Paris Tokyo

Professor Dr. MOHAN L. H. KAUL

Botany Department University, Kurukshetra Haryana -132119, India

ISBN-13: 978-3-642-83141-6 e-ISBN-13: 978-3-642-83139-3 DOl: 10.1007/978-3-642-83139-3

Library of Congress Cataloging-in-Publication Data. Kaui, Mohan L. H. Male sterility in higher plants. (Monographs on theoretical and applied genetics ; 10) Bibliography: p. Includes index. 1. Male sterility in plants. I. Title. II. Series. QK828.K38 1987 581.2'1662 87-14670

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© Springer-Verlag Berlin Heidelberg 1988 Softcover reprint of the hardcover I st edition 1988

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Monographs on Theoretical and Applied Genetics

Edited by R. Frankel (Coordinating Editor), Bet-Dagan M. Grossman, Urbana· H. F. Linskens, Nijmegen P. Maliga, Oakland . R. Riley, London

10

Monographs on Theoretical and Applied Genetics

Volume 1 Meiotic Configurations A Source of Information for Estimating Genetic Parameters By J. Sybenga

Volume 2 Pollination Mechanisms, Reproduction and Plant Breeding By R. Frankel and E. Galun

Volume 3 Incompatibility in Angiosperms By D. de Nettancourt

Volume 4 Gene Interactions in Development By L. 1. Korochkin

Volume 5 The Molecular Theory of Radiation Biology By K. H. Chadwick and H. P. Leenhouts

Volume 6 Heterosis Reappraisal of Theory and Practice Editor: R. Frankel

Volume 7 Induced Mutations in Plant Breeding By W. Gottschalk and G. Wolff

Volume 8 Protoplast Fusion Genetic Engineering in Higher Plants By y. Y. Gleba and K. M. Sytnik

Volume 9 Petunia Editor: K. C. Sink

Preface

" ...... Nature has something more in view than that its own proper males should

fecundate each blossom." Andrew Knight

Philosophical Transactions, 1799

Sterility implicating the male sex solely presents a paradoxical situation in which universality and uniqueness are harmoniously blended. It maintains a built-in outbreeding system but is not an isolating mechanism, as male steriles, the "self-emasculated" plants, outcross with their male fertile sibs normally. Both genes (nuclear and cytoplasmic) and environment, individually as well as conjointly, induce male sterility, the former being genetic and the latter nongenetic. Genetic male sterility is controlled either exclusively by nuclear genes (ms) or by the complementary action of nuclear (lr) and cytoplasmic (c) genes. The former is termed genic and the latter gene-cytoplasmic male sterility. Whereas genic male sterility exhibits Mendelian inheritance, gene-cytoplasmic male sterility is non-Mendelian, with specific transmissibility of the maternal cytoplasm type. Genetic male sterility is documented in 617 species and species crosses com­prising 320 species, 162 genera and 43 families. Of these, genic male sterility occurs in 216 species and 17 species crosses and gene-cytoplasmic male sterility in 16 species and 271 species crosses. The Predominance of species exhibiting genic male sterility and of species crosses exhibiting gene-cytoplasmic male sterility is due to the fact that for the male sterility expression in the former, mutation of nuclear genes is required, but in the latter, mutations of both nuclear and cytoplasmic genes are necessary. Since simultaneous or successive occurrence of both these mutations in a cell are rare, hybridization bringing the mutated cytoplasm and nuclear genome together and leads to gene-cytoplasmic male sterility. Little is known, however about the molecular interaction between the nuclear and cytoplasmic genes. Much circumstantial evidence, especially restriction endonucleases analysis, isolated in-vitro mitochondrial transla­tion products and drug and fungal toxin sensitivity implicate mitochondria as site of the cytoplasmic male sterility (c) gene. It is also evidenced by protoplast fusions permitting cytoplasmic transfer with or without mitochondria and chloroplast. Further confirmation of c gene location in mitochondrial genome is provided by the existence of intramitrochondrial DNA se­quences some of which behave as plasmids.

VI Preface

The book is written to embody the principles, concepts and details about male sterility known in 617 species and species crosses. It is divided into two parts. Part I includes principles, generalizations and fundamental concepts, chemical induction and environmental influence, critical discussions and specific conclusions on the nature, type, inheritance pattern, biochemis­try, molecular basis, major features, limitations, lacunae and breeding prospects of different male sterility types found in higher plants. Suppression of anther or viable pollen develop­ment and differentation infuses morphological, anatomical, phy­siological and biochemical alterations coupled with self-sterility. Details of all these facets are included. Descriptions of male sterility types, inheritance, gene action and control, chemical induction, breeding significance etc of individual plant species of various flowering families are presented in Part II. To facilitate location, species and their families are arranged in alphabetical order. For species, the traditional botanical name is used, fol­lowed by the less known new botanical names and by the common names and synonyms, placed in parenthesis. After a brief introduction of the genus or species, available details about various aspects of genic, gene-cytoplasmic and chemical male sterility are presented. In addition, the effect of chemicals and environment on male sterility induction and expression is described. The breeding value of male sterility is indicated for the economically useful species. Appropriately with each family, major findings like gene control, time and type of gene action, chemical influence etc, are tabulated to provide an insight into the known and unknown aspects of male sterility. The conclud­ing chapter includes concepts, facts, postulations, conclusions and recommendations about the known cases of male sterility listed in Table 55.5. For each species, the page number for reference in the text is given. Thus this table serves as an index of the species and species crosses in which male sterility is known and recorded in this book. The figures and tables obtained from various authors are adapted after modifications. References indexed are cited at the end. Due to the huge number of papers published in an increasingly large number of periodicals and in a multitude of languages, it was not possible to consult and include all the papers on male sterility. Moreover, to keep the monograph within reasonable bounds, a high degree of literature selection, with vast background read­ing, was necessary. To those researchers whose contribution has been excluded or inadequately represented, I express my apologies in the two words "pure ignorance". The responsibility for errors of commission and omission is mine. These, brought to my notice in a constructive manner, will be appreciated and acknowledged gratefully.

Preface VII

This book is dedicated to the scientists whose hard toil unravelled the intricacies of male sterility and set free its use for increased productivity.

Kurukshetra, India July 1987

Acknowledgements

MOHAN L. H. KAUL

To Professor Dr. H. F. Linskens, Botanisch Laboratorium, Nijmegen, the Netherlands, I am indebted for cooperation, encouragement, help and moral support especially during the difficult and frustrating period of past 4 years. His confidence in my work provided me with the motivation and stimulus to complete this book. The idea to work and write on male sterility owes its inception to my post-doctoral research (1972-74, 1978-1980) with Prof. W. Gottschalk, Bonn University, FRG, to whom I am grateful for inspiration and help, and to Prof. R. G. Palmer, Iowa State University Ames, USA, who offered me his personal collection of reprints and library facilities during 1981-1982. My heartfelt thanks to Ursula, Neelangini, Usha and Anjali, who were cheerful and unflappable in meeting the many demands on their time. My special thanks to scientists and researchers for promptly providing reprints and photographs of their publications used in this book. For transmission help, I thank Professor H. Schulte, Mr. J. B. H. Hoffmann and Dr. B. Brandi-Dohrn of DAAD. For printing, I thank the editorial staff of Springer-Verlag for their excellent cooperation and high technical assistance. To my family, I am grateful for their under­standing during the period of neglect.

MOHAN L. H. KAUL

Contents

Part I General Account

1

1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8

2

2.1 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 2.10 2.11 2.12 2.13 2.14

3

3.1 3.2 3.3 3.4 3.5 3.6 3.7

Introduction

Discovery. Occurrence Virtues .. Initial Reviews Definition and Concept Classification . . . . . Genetic Types Symbols Proffered and Abbreviations Used

Genic Male Sterility

Occurrence and Perpetuation . Mutagen-Induced ...... . Chromosome Loss or Addition Gene Control Types ........... . Gene Action ....... . Tapetal Form and Function . Environmental Influence . . Identification and Genetic Characterisation Breeding Value . . . . . . . . Development and Utilization . Maintenance and Perpetuation Contrivances to Usage Use in Breeding ....... .

Gene-Cytoplasmic Male Sterility

Introduction Occurrence Types .... Gene Control Gene Action Tapetum .. Environmental Influence

3

3 3 4 4 5 6

12 13

15

15 22 26 26 40 50 63 68 72 78 84 89 90 94

97

97 105 113 121 127 140 149

x

3.8 3.9 3.10

4

4.1 4.2 4.3 4.4

5

5.1 5.2 5.3 5.4 5.5 5.6 5.7 5.8 5.9

6

6.1 6.2 6.3

7

7.1 7.2 7.3 7.4

8

8.1 8.2 8.3

9

9.1 9.2

Sterile Cytoplasm Features Fertility Restoration Breeding Value ....

Chemical Male Sterility

Introduction ..... Chemical Gametocides Induced Sterility Male Gametocides

Biochemistry . . .

Amino Acids . . . Nucleic Acid Starvation . Carbohydrate - Protein Metabolism Cytokinin Content Enzyme Activity .... Enzyme Differences Micronutrient Deficiency Chlorophyll Content . . Biochemical Causes and Consequences .

Graft Transfer and Viral Nature

Transfer Across Grafts . . . . Viral Transmission . . . . . . Fungal and Insect Infestations

Molecular Basis .

c-Gene Location Mitochondrial Site Plasmid Role . . Chloroplast Site . .

Origin and Causes

Origin ..... . Proposed Causes Conclusions . .

Major Features

General Attributes Special Attributes .

Contents

158 171 176

193

193 193 213 213

221

221 224 225 225 226 229 229 231 231

233

233 235 239

240

240 240 244 247

248

248 250 257

258

258 263

Contents XI

10 Gynodioecy ........ 268

10.1 Genetic Control. . . . . . 269 10.2 Occurrence and Frequency 272 10.3 Sex Expression .... 272 10.4 Floral Size Differences 273 10.5 Maintenance 273 10.6 Conclusions . . . . . . 276

11 Utility, Limitations and Lacunae 278

11.1 Utility ........ 278 11.2 Concluding Remarks 282 11.3 Limitations 283 11.4 Lacunae ....... 284

Part n Flowering Families

12 Anacardiaceae .. 291

12.1 Anacardium occidentale . 291 12.2 Mangifera indica 291 12.3 Pistacia vera . 291 12.4 Rhus .... 292

13 Begooiaceae 293

13.1 Begonia semperflorens 293

14 Cannaceae 295

14.1 Canna glauca 295

15 Cannabinaceae 296

15.1 Cannabis sativa 296 15.2 Humulus lupulus 297

16 Caricaceae .. 298

16.1 Carica papaya . 298

17 CaryopbyUaceae 299

17.1 Dianthus 299 17.2 Silene ...... 300

XII

18

18.1 18.2 18.3

19

19.1 19.2 19.3 19.4 19.5 19.6 19.7 19.8 19.9 19.10 19.11

20

20.1 20.2 20.3 20.4 20.5 20.6

21

21.1 21.2 21.3 21.4

22

22.1

23

23.1 23.2 23.3 23.4

Chenopodiaceae ......... .

Beta . ............... . Chenopodium quinoa Wild (quinea) Spinacea deracea L. (Spinach)

Compositae . . . . .

Ageratum ..... . Carthamus tinctorius Centaurea .... Chrysanthemum. . Cirsium ..... . Helianthus annuus Lactuca ... Parthenium Tagetes erecta Taraxacum Zinnia elegans .

Cruciferae . . .

Arabidopsis thaliana Brassica ..... . Cheiranthus cheiri . Daucus carota . . Eruca sativa . . . Raphanus sativus

Cucurhitaceae . .

Bryonia ..... Citrullus vulgaris Cucumis . Cucurbita

Ericaceae

Vaccinium angustifolium

Euphorhiaceae

Hevea brasiliensis Manihot esculenta M ercurialis .. . Ricinus communis .

Contents

302

302 328 328

329

329 334 335 335 336 337 350 352 353 354 355

356

356 356 382 383 390 390

393

393 395 397 401

411

411

412

412 413 413 416

Contents

24

24.1

25

25.1 25.2

26

26.1 26.2

27

27.1 27.2 27.3 27.4 27.5 27.6 27.7 27.8 27.9 27.10 27.11 27.12 27.13 27.14 27.15 27.16 27.17 27.18 27.19 27.20 27.21

28

28.1

29

29.1 29.2 29.3 29.4 29.5

Fagaceae

Castanea

Geraniaceae

Geranium .. Pelargonium

Gesneriaceae

Kohleria . .. Streptocarpus

Gramineae

Aegilops .. Agroelymus turneri Alopecurus myosuroides Avena . ...... . Chionachne koenigii . Dactylis glomerata . Echinocloa colone . Eleusine ..... . Festuca arundinacea Hordeum vulgare Lolium ..... . Oryzasativa ... . Pennisetum typhoides Phleum .. . Saccharum .. . Secale cereale . . Sorghum vulgare Tragopogon . . . Tripsacum laxum Triticum. Zeamays

lridaceae

Iris ...

Labiatae

Coleus .. Lavandula angustifolia Origanum . .. . Salvia ..... . Satureja hortensis

XIII

418

418

419

419 420

426

426 427

431

431 432 432 433 435 435 436 436 436 437 455 459 481 492 492 493 501 516 517 517 551

615

615

617

617 619 619 621 622

XIV

30

30.1 30.2 30.3 30.4 30.5 30.6 30.7 30.8 30.9 30.10 30.11 30.12 30.13 30.14 30.15 30.16 30.17

31

31.1 31.2

32

32.1

33

33.1

34

34.1 34.2 34.3

35

35.1 35.2

36

36.1

Leguminosae . .

Arachis hypogaea Cajanus cajan . . Crotalaria . . . . Desmodium sandwicense Glycine max . Lathyrus ... Lens culinaris Lotus filicaulis . Lupinus .... Medicago sativa Melilotus alba Phaseolus Pisum .. Trifolium Viciafaba Vigna Wisteria .

Liliaceae

Allium Kniphofia

Limnanthaceae

Limnanthes douglasii

Linaceae ..... .

Linum usitatissimum

Malvaceae

Abelmoschus Gossypium Thespesia populnea

Moraceae .

Ficus ... Morusnigra

Myrsinaceae

Rapanea thwaitesii .

Contents

623

623 624 627 628 629 644 645 646 646 647 655 655 657 662 664 676 678

685

685 696

698

698

699

699

705

707 707 716

717

717 717

718

718

Contents XV

37 Oleaceae .. 719

37.1 Olea europea 719 37.2 J asminum pubescens 719

38 Onagraceae . . . 720

38.1 Epilobium . ... 720 38.2 Godetia whitneyi 726 38.3 Oenothera .. 726

39 Papaveraceae 728

39.1 Argemone mexicana . 728 39.2 Papaver somniferum 728

40 Pedaliaceae . . . 729

40.1 Sesamum indicum 729

41 Plantaginaceae 732

41.1 Plantago 732

42 Polemoniaceae 735

42.1 Gilia ..... 735 42.2 Polemonium caeruleum 735

43 Polygonaceae . . . . . 736

43.1 Fagopyrum esculentum 736 43.2 Rumex acetosa 736

44 Primulaceae . . 737

44.1 Cyclamen persicum 737 44.2 Primula .... 737

45 Ranunculaceae 738

45.1 Aquilegia 738 45.2 Ranunculus 739

46 Rosaceae 741

46.1 Fragaria . 742 46.2 Malus sylvestris 742

XVI Contents

47 Rutaceae 743

47.1 Citrus .. 743

48 Scrophulariaceae 747

48.1 Antirrhinum majus 747 48.2 Hebe .. 749 48.3 Veronica 749

49 Solauaceae 750

49.1 Capsicum annuum 750 49.2 Datura strmonium . 758 49.3 L ycopersicon esculentum 758 49.4 Nicotiana 775 49.5 Petunia 798 49.6 Solanum 811

50 Tiliaceae 838

50.1 Corchorus capsularis 838

51 Urticaceae 839

51.1 Pilea microphylla 839

52 Valerianaceae . . 840

52.1 Centranthus ruber 840 52.2 Valeriana officinalis 840

53 Violaceae 841

53.1 Viola .. 841

54 Vitaceae 843

54.1 Vitis ... 843

55 Concepts and Conclusions . 845

55.1 Concepts ..... 845 55.2 Conclusions . . . . 861 55.3 Recommendations 861

References. . ....... 885

Subject index 993