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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