Apomixis in Angiosperms: Mechanisms, Occurrences, and Biotechnology

275 Pages·2022·14.837 MB·English

by  Diego Hojsgaard, Thammineni Pullaiah

Apomixis in Angiosperms
Apomixis is a difficult-to-analyse trait with a complex molecular basis and a substantive effect on
the biology of a species. Thus, apomixis is an interesting characteristic for researchers and students
working in different fields of plant science and agriculture and technological advances are enabling
and making apomixis studies more common.
Apomixis in Angiosperms: Mechanisms, Occurrences, and Biotechnology provides a system-
atic introduction to the mechanisms and developmental types of apomixis along with an overview of
alternative methodologies for identifying apomixis and a detailed reassessment of the occurrences
of apomictic species among angiosperm families. Optional methods are illustrated with examples of
all types of apomixis and biological levels of analysis, i.e. cells, ovules, seeds and offspring. Data on
apomictic species are collected in tables along with information on ploidy, type of apomixis and ref-
erences. Occurrences of apomixis are briefly discussed in phylogenetic and evolutionary contexts.
An outline of the molecular basis of apomixis in plants is presented, together with prospects and
challenges that remain for its biotechnological exploitation.
This book:
• Provides a systematic overview of the mechanisms of apomixis, developmental types and
methodology for apomixis research.
• Reassesses apomixis at the species level in angiosperm families.
• Contains tables summarizing relevant information on apomixis.
• Analyses occurrences of apomixis in phylogenetic and evolutionary contexts.
• Outlines the molecular basis and biotechnological perspective of apomixis breeding.
This book presents an accessible overview of apomixis research and a curated dataset of apomictic
species. It serves as a reference book for students, researchers and citizen scientists interested in
apomixis, as well as researchers, business innovators and entrepreneurs pursuing apomixis breed-
ing. It can also be used as a textbook in graduate courses on plant reproduction.
Diego Hojsgaard Taxonomy and Evolutionary Biology, Leibniz Institute of Plant Genetics and
Crop Plant Research, Gatersleben, Germany, and Faculty of Exact, Chemical and Natural Sciences,
National University of Misiones, Posadas, Argentina.
Thammineni Pullaiah Department of Botany, Sri Krishnadevaraya University, Anantapur, India.

Apomixis in
Angiosperms
Mechanisms, Occurrences, and Biotechnology
Diego Hojsgaard
Thammineni Pullaiah
Cover image: Mountain meadow at about 2100 m.a.s.l. with apomictic daisies and grasses near Santa Cruz (Tafí del Valle),
northwestern Argentina in South America. Behind is the Cerro Pelao covered in clouds.
First edition published 2023
by CRC Press
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© 2023 Diego Hojsgaard and Thammineni Pullaiah
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ISBN: 978-0-367-54295-5 (hbk)
ISBN: 978-0-367-54296-2 (pbk)
ISBN: 978-1-003-08856-1 (ebk)
DOI: 10.1201/9781003088561
Typeset in Times
by SPi Technologies India Pvt Ltd (Straive)
Contents
Preface ...............................................................................................................................................ix
Authors ..............................................................................................................................................xi
Chapter 1 Introduction ..................................................................................................................1
Chapter 2 Sexual Development and Pathways to Apomixis .........................................................5
2.1 Introduction .......................................................................................................5
2.2 The Sexual Pathway of Seed Formation ............................................................6
2.2.1 The Female Gametophyte ....................................................................6
2.2.2 The Male Gametophyte ........................................................................7
2.2.3 The Progamic Phase: From Pollination to Double Fertilization ..........7
2.2.4 The Making of a Seed: Embryo and Endosperm Formation ................8
2.3 Main Features of Sexual Reproduction .............................................................8
2.4 Apomixis and the Alternatives to Sexual Seeds ................................................9
2.4.1 Sporophytic Apomixis ..........................................................................9
2.4.1.1 Initial Cell Growth and Embryo Formation ........................10
2.4.1.2 Sexual Development in Sporophytic Apomicts ..................10
2.4.1.3 Main Features of Sporophytic Apomixis ............................11
2.4.2 Gametophytic Apomixis .....................................................................12
2.4.2.1 Diplosporous Developments ...............................................12
2.4.2.2 Aposporous Developments .................................................14
2.4.2.3 Sexual Development and Embryo and Endosperm
Formations in Diplosporous and Aposporous Apomicts ......16
2.4.2.4 Main Features of Gametophytic Apomixis .........................18
2.5 Common Facts among Apomicts .....................................................................18
2.6 Other Deviations from Sexual Reproduction ..................................................18
Chapter 3 Identifying Apomixis in Nature ..................................................................................19
3.1 Introduction .....................................................................................................19
3.2 Detecting Apomixis in Flowers and Ovules ....................................................19
3.2.1 Embryology and the Identification of Apomixis Types ......................19
3.2.1.1 Embryological Methods ......................................................21
3.2.1.2 Callose Deposition ..............................................................21
3.2.1.3 The Auxin Test for Parthenogenesis ...................................22
3.2.2 Testing the Autonomous Development of Seeds ................................23
3.2.2.1 Pollen Exclusion Tests ........................................................23
3.2.2.2 Castration Experiments .......................................................24
3.3 Detecting Apomixis in Seeds ...........................................................................24
3.3.1 Germination Tests ...............................................................................24
3.3.2 Flow Cytometric Seed Screen ............................................................25
3.3.3 Endosperm Storage Proteins ..............................................................28
3.4 Detecting Apomixis in Plants and Progenies ...................................................28
3.4.1 Progeny Tests ......................................................................................28
3.4.1.1 Morphological Evaluation ..................................................29
v
vi Contents
3.4.1.2 Cytological Evaluation .......................................................29
3.4.1.3 Molecular Evaluation ..........................................................29
3.4.2 Marker-Assisted Selection to Screen for Apomixis in Plants ............30
3.5 Studying Apomixis-Associated Features .........................................................31
Chapter 4 Apomictic Grasses ......................................................................................................33
4.1 Introduction .....................................................................................................33
4.2 Considerations on the Occurrence and Type of Apomixis in Grasses .............33
4.2.1 Doubtful Cases of Apomixis in Grasses .............................................45
4.3 Pathways to Asexual Seeds in Grasses ............................................................47
4.3.1 Sporophytic Apomixis in Grasses ......................................................48
4.3.2 Gametophytic Apomixis in Grasses ...................................................48
4.3.2.1 The Aposporous Development ............................................48
4.3.2.2 The Diplosporous Development .........................................49
4.3.2.3 Variations in Female Gametophyte Ontogeny and
Anatomy .............................................................................50
Chapter 5 Apomictic Daisies ......................................................................................................51
5.1 Introduction .....................................................................................................51
5.2 Considerations about the Occurrence and Type of Apomixis in Daisies .........51
5.2.1 Doubtful Cases of Apomixis in Daisies .............................................69
5.3 Pathways to Asexual Seeds in Daisies .............................................................72
5.3.1 Sporophytic Apomixis in Daisies .......................................................74
5.3.2 Gametophytic Apomixis in Daisies ....................................................74
5.3.2.1 The Aposporous Development ............................................74
5.3.2.2 The Diplosporous Development .........................................74
5.3.2.3 Variations in Female Gametophyte Ontogeny and
Anatomy .............................................................................75
Chapter 6 Apomictic Roses ........................................................................................................77
6.1 Introduction .....................................................................................................77
6.2 Considerations about the Occurrence and Type of Apomixis in Roses ...........77
6.2.1 Doubtful Cases of Apomixis in Roses ................................................94
6.3 Pathways to Asexual Seeds in Roses ...............................................................98
6.3.1 Sporophytic Apomixis in Roses .........................................................98
6.3.2 Gametophytic Apomixis in Roses ......................................................99
6.3.2.1 The Aposporous Development ............................................99
6.3.2.2 The Diplosporous Development .........................................99
6.3.2.3 Variations in Female Gametophyte Anatomy and
Maturity ............................................................................100
Chapter 7 Apomixis in Other Families of Angiosperms ...........................................................101
7.1 Introduction ...................................................................................................101
7.2 Considerations on the Occurrence and Type of Apomixis in
Distinct Families ............................................................................................102
7.2.1 Doubtful Cases of Apomixis in Different Plant Families .................132
7.3 Pathways to Asexual Seeds in Other Plant Families .....................................139
Contents vii
7.3.1 Sporophytic Apomixis ......................................................................140
7.3.1.1 Nucellar Embryony ...........................................................140
7.3.1.2 Integumentary Embryony .................................................142
7.3.2 Gametophytic Apomixis ...................................................................143
7.3.2.1 The Aposporous Development ..........................................143
7.3.2.2 The Diplosporous Development .......................................143
7.3.3 Variations in the Development of Asexual Seeds .............................145
Chapter 8 Apomixis in Angiosperms ........................................................................................149
8.1 Introduction ...................................................................................................149
8.2 Apomixis in Angiosperms .............................................................................149
8.2.1 Phylogenetic Distribution of Apomixis ............................................150
8.2.2 Ranking of Apomictic Families and Prevalence of
Apomictic Types ...............................................................................150
8.2.3 Apomixis and Endosperm Development ..........................................153
8.2.4 Apomixis and Ploidy ........................................................................153
8.3 Apomixis and Sexuality.................................................................................155
8.4 Taxonomic Issues Raised by Apomixis and Species Delimitations ..............157
8.5 Apomixis and Evolution ................................................................................158
Chapter 9 Molecular Basis of Apomixis and Applications .......................................................161
9.1 Introduction ...................................................................................................161
9.2 Apomixis in Plant Breeding ..........................................................................162
9.3 Genetics of Apomictic Development .............................................................163
9.3.1 Sporophytic Apomixis ......................................................................163
9.3.2 Gametophytic Apomixis ...................................................................164
9.4 Apomixis Technology: The Quest for the Molecular Basis of Apomixis .....168
9.5 Apomixis for Backing Up Genetic Diversity ................................................171
Glossary ........................................................................................................................................173
References .....................................................................................................................................175
Index ..............................................................................................................................................247

Preface
Advances in apomixis research over the past three decades have been remarkable, and the com-
ing decades look auspicious. Increasingly easy access to molecular biology and flow cytometry
methods, coupled with a plethora of open-source bioinformatics software for intuitive visualization,
exploration and integration of biological data that require less and less programming knowledge,
memory and processing power, is helping researchers characterize apomixis at many levels. Despite
limited funding, apomixis scientists are currently exploring – with outstanding results – all major
types of biological data for meta-analysis in molecular biology, ecology and evolutionary biology.
Outstanding in recent discoveries is the identification and functional characterization of genes
that trigger components of apomixis or apomixis-like phenotypes. A noteworthy shift of paradigm
is the growing recognition of apomixis as an evolutionary force that plays an active role in the main-
tenance and diversification of species. Remaining challenges concern the unresolved taxonomic
consent on the criteria for delimiting species with apomixis, understanding the genetics underlying
the ecological adaptation of apomicts and the dynamics of apomixis to sex reversals in nature, and
unravelling the molecular basis for the occurrence of the trait.
Scientists investigating apomixis are now – more than ever – faced with the need to join forces
and cooperate on different fronts to consolidate apomixis as a model in evolutionary studies and as
a biotechnological tool in molecular breeding. Honest engagement, fair peer review and good data
management and stewardship would be the keys to facilitating this path.
Sincere gratitude to those colleagues who helped in one way or another during the process of this
book, whether by sharing invaluable ideas and discussions, assisting with some of the illustrations,
embryological classifications or taxonomic identifications, or providing literature. We are indebted
to Drs Silvia Arroyo-Leuenberger, Ana Caperta, John Carman, Julio Daviña, Timothy Dickinson,
Angel Hojsgaard, Ana Honfi, Elvira Hörandl, Piyal Karunarathne, Eric Martínez, Patrik Mráz,
Kristina Musiał, Camilo Quarin, Agostina Sassone, Jan Štěpánek and Peter van Dijk.
We also thank Jyotsna Jangra and Renu Apadhyay, from CRC Press, for their assistance in bring-
ing this edition to print.
Diego Hojsgaard
Aschersleben, Germany
Thammineni Pullaiah
Anantapur, India
ix