Plant Transposons and Genome Dynamics in Evolution E-Book

• Herausgeber: John Wiley & Sons
• Kategorie: Wissenschaft und neue Technologien
• Sprache: Englisch

Seitenzahl: 575

Veröffentlichungsjahr: 2013

Beschreibung

The transposable genetic elements, or transposons, as they are now known, have had a tumultuous history. Discovered in the mid-20th century by Barbara McClintock, they were initially received with puzzlement. When their genomic abundance began to be apparent, they were categorized as "junk DNA" and acquired the label of parasites. Expanding understanding of gene and genome organization has revealed the profound extent of their impact on both. Plant Transposons and Genome Dynamics in Evolution captures and distills the voluminous research literature on plant transposable elements and seeks to assemble the big picture of how transposons shape gene structure and regulation, as well as how they sculpt genomes in evolution. Individual chapters provide concise overviews of the many flavors of plant transposons and of their roles in gene creation, gene regulation, development, genome evolution, and organismal speciation, as well as of their epigenetic regulation. This volume is essential reading for anyone working in plant genetics, epigenetics, or evolutionary biology.

Leseprobe

Contents

Cover Page

Title Page

Copyright

Contributors

Foreword

Introduction

Chapter 1: The Discovery of Transposition

Introduction

Studies on Variegation

Mutable Genes

McClintock’s Studies on Chromosome Breakage

Recognition that Ds Transposes

Explaining Mutable Genes

Molecular Endnote

References

Chapter 2: A Field Guide to Transposable Elements

The C-value Paradox

The Quantity of Transposable Elements Determines Genome Size

General Classification Scheme for Transposable Elements

Class II Elements

Class I: The Non-LTR and LTR Retrotransposons

Evolutionary Origins of Transposable Elements

Non-autonomous Transposable Elements

Transposable Element Demography and Genome Ecology

Conclusions: Rehabilitation of Transposable Elements

Acknowledgments

References

Chapter 3: The Mechanism of Ac/Ds Transposition

Transposition of Ac/Ds Elements

The Enigmatic Ac Dosage Effect

cis and trans Effects on Ac/Ds Transposition

Molecular Characterization of Transposable Elements

The Excision and Insertion Reactions

Formation of Ds from Ac

Standard versus Alternative Transposition

Sister Chromatid Transposition

Reversed-ends Transposition

How Does Ds Break Chromosomes?

Alternative Transposition, DNA Methylation, and the Sequence of Transposition Reactions

Potential Applications of Alternative Transposition

Perspective

References

Chapter 4: McClintock and Epigenetics

Introduction

Spm-suppressible Alleles

Spm-dependent Alleles

Cryptic Spm

Presetting

Molecular Machinery of Epigenetic Regulation

Summary

References

Chapter 5: Molecular Mechanisms of Transposon Epigenetic Regulation

Introduction

Chromatin Remodeling, DNA and Histone Modification

RNA Interference (RNAi) and RNA-Directed DNA Methylation (RdDM)

Heterochromatin Reprogramming and Germ Cell Fate

Transgenerational Inheritance of Transposon Silencing

Paramutation

Conclusions

References

Chapter 6: Transposons in Plant Gene Regulation

Introduction

New Regulatory Functions

TE-Induced Down-Regulation

Deletions and Rearrangements

Suppressible Alleles

TEs and Plant Domestication

The Dynamic Genome

References

Chapter 7: Imprinted Gene Expression and the Contribution of Transposable Elements

Why are Genes Imprinted?

The Developmental Origin of Endosperm

Selection for Imprinted Expression

Principles Derived from the First Imprinted Gene

Gene Imprinting and Parent-of-Origin Effects on Seed Development

What Genes are Imprinted?

Epigenome Dynamics during Seed Development

Epigenetic Landscape in Vegetative Tissues

Cytological Observations of Chromatin in Seeds

Epigenomic Profiling in Seeds

Mechanisms of Gene Imprinting and the Relation to TEs

TEs and Allele-Specific Imprinting

Insights from Whole Genome Studies

Outstanding Questions

References

Chapter 8: Transposons and Gene Creation

Introduction

Capture of Gene Fragments by TEs and Formation of Chimeric Genes

Co-Option of a TE Gene by the Host

Fusion of TE and Host Genes

Alterations of Host Gene Sequences by TE Excisions

Alterations of Host Coding Sequences by TE Insertions

Acquisition by Host Genes of New Regulatory Sequences from TEs

Interaction of TEs with Target Gene mRNA Splicing and Structure

Reshuffling of Host Sequences by Alternative Transpositions

Conclusion

References

Chapter 9: Transposons in Plant Speciation

Introduction

Speciation Through Accumulation of Mutations

Plant Speciation Through Hybridization and Allopolyploidization

A Mechanistic Model for Responses to Genome Shock

Conclusions

Acknowledgments

References

Chapter 10: Transposons, Genomic Shock, and Genome Evolution

How Transposons Came to be Called “Selfish” DNA

Sequence Duplication: The Real Innovation

Plant Genome Organization: Gene Islands in a Sea of Repetitive DNA

References

Index

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Contributors

Jeffrey L. BennetzenDepartment of Genetics, University of Georgia, Athens, Georgia, USADavid BotsteinLewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USAVicki L. ChandlerGordon and Betty Moore Foundation, Palo Alto, California, USAHugo K. DoonerWaksman Institute, Rutgers University, New Jersey, USANina V. FedoroffKing Abdullah University of Science and Technology, Thuwal, Saudi Arabia and Pennsylvania State University, Pennsylvania, USAMary A. GehringWhitehead Institute and Massachusetts Institute of Technology, Cambridge, Massachusetts, USAAvraham A. LevyDepartment of Plant Sciences, Weizmann Institute of Science, Rehovot, IsraelDamon R. LischDepartment of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USARobert A. MartienssenHoward Hughes Medical Institutes, New York, New York, USA and Gordon and Betty Moore Foundation, Palo Alto, California, USA and Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USAThomas PetersonDepartment of Genetics, Development and Cell Biology and Department of Agronomy, Iowa State University, Ames, Iowa, USAAlan H. SchulmanMTT Agrifood Research Finland and Institute of Biotechnology, University of Helsinki, Helsinki, FinlandClifford F. WeilDepartment of Agronomy, Purdue University, West Lafayette, Indiana, USAThomas WickerInstitute of Plant Biology, University of Zurich, Zurich, SwitzerlandJianbo ZhangDepartment of Genetics, Development and Cell Biology, Iowa State University, Ames, Iowa, USA

Foreword

David Botstein

Science is both a rational and a social endeavor. The basic paradigm for scientific progress, comprising a progression from observation to theory and experimentation, has been in place for several hundred years. Mostly science moves in steps small enough so that the introduction of a new idea, theory, or point of view is followed fairly quickly by a consensus among scientists who become convinced by the evidence. Scientists are taught to value new ideas and to evaluate the evidence, even when new ideas are revolutionary and fundamental. Often they have no difficulty doing so: Einstein’s astonishingly original ideas were understood and largely accepted by physical scientists within a decade or so of their publication.

Occasionally, however, there are geniuses who make observations, propose theories, and carry out convincing experiments that are somehow so far in advance of contemporary scientific understanding that the general acceptance of their ideas, even by the scientific community, lags for many decades. The work of three well-known giants in the history of biology displayed this kind of intellectual “prematurity”: Charles Darwin, Gregor Mendel, and Barbara McClintock.

This book is a compendium of what is known and accepted today about transposons and genomic dynamics in plants, a field whose basic ideas manifestly derive from the work and insights of Barbara McClintock to a degree similar to the influence of Mendel on genetics and Darwin on evolution. As with Darwin and Mendel, acceptance of McClintock’s ideas has taken many decades. But unlike Darwin and Mendel, the depth of her insight is still to be fully appreciated.

What stood in the way? Some of McClintock’s discoveries, such as the relationship between chromosomes and linkage groups, achieved immediate acceptance. Transposition, by contrast, took decades and repeated rediscovery in organisms other than maize. Still others, such as the concept that genomes sense and respond to external stimuli, are just beginning to find experimental support and intellectual acceptance.

The barrier was not obscurity or even gender. McClintock achieved a high status early in her career on the basis of her achievements. Unlike Mendel, she and her ideas were well known and widely accepted in her community. Despite her eminence, other scientists appear simply to have failed to understand some of her ideas or the evidence on which they were based. Unlike the case of Darwin, there were no religious or ideological barriers to the acceptance of McClintock’s ideas. Hers seems to have been purely a matter of having been ahead of her time.

But I also believe that two commonly held convictions had to change to make way for full acceptance of McClintock’s ideas about genome dynamics in evolution, which are the subject of this book. The first was the generalization that only proteins and their regulation are really important in understanding biology and evolution. The second was the conviction that the mechanisms of evolution could not themselves evolve.

The focus on proteins was entirely understandable: it was at the heart of the molecular biology revolution. Molecular biologists explicitly taught the “central dogma” that information flows from DNA to RNA to protein and only thence to phenotype and fitness. No surprise, then, that the biological community sought to understand everything in terms of proteins and their regulation. This led to an unwanted and, and surely unintended consequence: dismissal of noncoding DNA as “junk.” Of course, this “junk” included all the transposons and transposon remnants that, as readers of this book will see, are what make the genome dynamic and are the drivers of genome evolution.

The misunderstanding about evolution of evolutionary mechanisms arose from the long-running debate about Darwinism, not only among scientists, but also in society more generally. Countering religious rejection of Darwinism in favor of divine intention and teleological arguments, scientists rather vehemently rejected the legitimacy of teleology in scientific reasoning. This rejection led, perhaps unwittingly, to the dismissal of “evolvability” as a property that could be selected in evolution. For most of the twentieth century, the scientific community treated the concept of evolvability as requiring something like intention or, at least, precognition.

The idea that one genome is more fit than another because it is more mutable was an idea that, at best, was hard to imagine. The dismissal of transposons as “junk” DNA and as “parasites” whose destructiveness genomes must rigidly control also interfered with perception of their contribution to evolvability. Thus in order for McClintock’s ideas about genome dynamism to be accepted, it was first necessary for the scientific community to assimilate the existence and sheer genomic abundance of transposons and then to appreciate their agency in the mechanisms of chromosome mechanics and functional evolution.

This book is a thorough examination of the current state of knowledge about the numbers and nature of transposons and retrotransposons and how they have shaped plant genomes. Progress of this more incremental variety has come through the invention and application of rapid techniques for genome and transcript analysis. The results have led to a renewed appreciation that Barbara McClintock understood much more than the basic ideas of chromosome mechanics and transposition, both of which were already widely accepted by the time of her death in 1992.

Indeed, McClintock discovered and recognized the significance of what we now call “epigenetics” – the heritable, reversible regulation of gene activity. The study of epigenetics and epigenomics has only recently become one of the hottest research fields of our time. The larger community is just now beginning to assimilate fully the notion that phenotypes reflect not only genotypes but also the epigenetic consequences of both development and response to the environment. Finally, and perhaps most importantly, McClintock understood, as the rest of us are only beginning to figure out, that there are well-orchestrated genomic stress responses that can rapidly restructure genomes – the quintessence of evolvability.

Introduction

Nina V. Fedoroff

McClintock’s discovery of transposition in the middle of the twentieth century was roughly contemporaneous with Watson and Crick’s landmark elucidation of DNA structure. But although Watson and Crick were recognized with a Nobel Prize within a decade, several more decades elapsed before the importance of McClintock’s work on transposons was recognized with the award of an unshared Nobel Prize. The mystery of why it took so long for transposable genetic elements to be recognized as something more than a genetic oddity is dissipating as we increasingly appreciate the role of epigenetic mechanisms in silencing transposons and maintaining chromosome stability. Given the current recognition of their importance, it is curious that the study of DNA methylation and other epigenetic mechanisms has only recently advanced from the status of mildly disreputable to the cutting edge of investigation.

The term “transposable element” (TE) is generally used here to refer to both transposons that move through a DNA intermediate and retrotransposons that move through an RNA intermediate. The present volume seeks to capture and distill the veritable mountain of information that has now accumulated on the many flavors of plant TEs, their genetics, genomics, and epigenetics. It also provides an opportunity to indulge in a bit of hindsight, with its extraordinary acuity, and to reassess the larger picture of transposons in gene structure and regulation, as well as in genome and organismal evolution.

Although she is best known for her discovery of transposable genetic elements, recounted in Chapter 1, McClintock’s contributions went well beyond transposition. Her seminal work on epigenetic regulation, described in Chapter 4, remains largely unrecognized, as do her insights into genome restructuring. Indeed, it became fashionable to discredit McClintock’s view that transposons are gene regulators. And yet, although she did not get everything exactly right, her early insights seem remarkably prescient from a contemporary vantage point, compelling a rethinking of both regulation and the relationships among the genome’s indigenous gene populations.

Early in her work on transposons, McClintock came to the conclusion that they were unmoored gene regulatory systems that had become associated with different genes by virtue of their ability to move. This view was reinforced by her growing appreciation that a single active transposon could promote excision of transposition-defective elements belonging to the same family from insertion sites in several genes simultaneously. This hierarchical relationship, in turn, reinforced her conviction that transposons were integral parts of the developmental regulatory machinery and she therefore named them “controlling elements.”

She viewed transposons as bits of heterochromatin by analogy to the connection between heterochromatin and certain types of variegated gene expression in Drosophila. In a 1950 paper published in the Proceedings of the National Academy of Sciences, she wrote:

Changes in quantity, quality or structural organization of heterochromatic elements may well alter the kind and/or degree of particular exchanges that occur, and in this way control the chromosome organization and the kind and the relative effectiveness of genic action.

This has turned out to quite close to the contemporary recognition that large blocks of silenced and recombinationally inert retrotransposons separate small “islands” of genes in many plant genomes, as discussed in detail in Chapters 2 and 10.

McClintock’s intense study of the Suppressor-mutator (Spm) transposon, described in Chapter 4, produced the first detailed genetic characterization of an epigenetic regulatory system, further expanding the range of transposon regulatory attributes that could influence expression of a gene into which a transposon had inserted.

Contemporary concepts of gene regulation are rooted in the pioneering work of Jacob and Monod on bacterial genes. Although McClintock’s assessment of the parallels between the prokaryotic and eukaryotic regulatory systems appears quite accurate in retrospect, her views gained little traction at the time, perhaps because the gene regulatory story was confounded by transposition, a phenomenon that had not yet been discovered in bacteria. But writing in the American Naturalist in 1961, McClintock said:

It should be emphasized that, although transposition of controlling elements in maize made it possible to recognize their presence in the chromosome complement and to study the mode of operation of the component elements of a system, transposition does not necessarily characterize the behavior of a controlling element. An element previously exhibiting transposition may become fixed in a location. If it is the gene-associated element that becomes fixed, the action of the gene will then be permanently under the control of the system to which the element belongs.

We now know that precisely such regulatory captures underlie the various phenotypes of Spm insertion mutations (Chapter 4). More that that, we know that such captures are a regular feature of gene evolution in plants, so much so that it has been proposed that all epigenetic regulation of plant genes derives from transposons (Chapters 6–8).

By the time McClintock wrote the 1961 American Naturalist article comparing bacterial and maize gene regulatory systems, her understanding of the Spm transposon’s genetic regulatory mechanism had advanced well beyond anything that had then been described in either prokaryotes or eukaryotes. In retrospect, it is clear that the complexity of McClintock’s description arose primarily from the fact that the Spm element is regulated by both epigenetic modification and the transposon’s regulatory system. As a result, insertions of different transposition-defective elements at different positions in the gene and promoter regions of the pigment biosynthetic genes that served her as reporter genes gave alleles with a remarkable variety of phenotypes (Chapter 4).

What is extraordinary is her insight that the trans-acting Spm transposon itself could undergo changes in expression that were heritable, but reversible – what we now call epigenetic. In the same American Naturalist article, she wrote:

One of the most interesting and theoretically important types of expression of Spm consists in the sequentially occurring reversals in phase of its activity – from active to inactive and back to active. …Following such a reversal of phase, the duration of the particular phase may be long, continuing unaltered through many cell or even plant generations, or it may be short, reversal occurring again in a number of cells only a relatively few cell generations removed from that which initiated the preceding phase. Control of duration of a particular phase appears to be associated with the event that produces the particular reversal of phase. By selective methods, it has been possible to isolate Spm displaying either a long duration of an active phase or a long duration of an inactive phase.

More than that, she reported that an active Spm transposon could activate an epigenetically inactive one, suggesting that the transposon encodes its own epigenetic activator, subsequently identified as the transposon-encoded TnpA protein and shown to function precisely as predicted from the genetic interactions (Chapter 4).

We now know that epigenetic silencing is accomplished by a complex of mechanisms that includes histone modification, RNA interference, and RNA-directed DNA methylation. DNA methylation is reversed by both passive and active mechanisms, and reactivation of silent transposons occurs under a variety of conditions, as described in Chapter 5. Although recent experiments suggest that there is gene- and transposon-specificity in epigenetic silencing and reactivation, the Spm transposon’s epigenetic regulatory mechanism remains among the very few that have been extensively investigated to date, either genetically or at the molecular level.

The invention and perfection of DNA sequencing techniques in the late 1970s set the stage for the subsequent rapid expansion of knowledge about the structure, gene content, and organization of genomes. During the debates that took place at the time about whether it was worth sequencing complete genomes in view of the suspicion that much of the DNA was repetitive and did not code for either proteins or the then-known structural RNAs, transposons were lumped with other kinds of repetitive sequences and given Ohno’s and Dawkins labels of “junk” and “selfish” DNA based on the view that they existed solely to propagate themselves and made no contribution to genome structure or function.

Angiosperm genomes, like the genomes of other higher eukaryotes, vary widely in their haploid DNA content, even within a single species, a phenomenon long known as the C-value paradox. We now know that, indeed, this wide C-value disparity is attributable to the differential accumulation of transposons and retrotransposons, predominantly the latter (Chapters 2 and 10). At the same time, it has become increasingly clear that the organization and evolution of higher plant genomes are driven largely by transposons and retrotransposons.

Astonishingly, the vast majority of the DNA in higher plants comprises transposons and retrotransposons: 85% of the maize genome, for example, consists of TEs, predominantly retrotransposons. The typical large angiosperm genome exhibits small “islands” of genes in a “sea” of repetitive DNA, primarily consisting of retrotransposons (Chapter 10). Although there is significant constancy of total gene numbers and retention of gene complements, the colinearity of homologous genes declines with evolutionary distance and intergenic regions change rapidly (Chapter 10). Comparisons even among inbred strains of maize reveal substantial differences in gene organization and even larger differences in both the length of intergenic regions and their content of transposons and retrotransposons (Chapter 10). Whole genome comparisons across species suggest that both the movement of genes and the intergenic churn are caused by transposons and retrotransposons. Whether examining the results of transposition events involving a single transposon (Chapter 3) or viewing the contribution of transposons to the evolution of chromosomes (Chapter 10), the centrality of transposons to contemporary genome organization is inescapable.

Transposons make many subtle contributions to gene and genome evolution, as well. Transposons create genes, modify them, and program and reprogram their expression (Chapters 7–10). The traffic in genes and regulatory sequences is bidirectional: transposons pick up genes that code for proteins other than transposases and transposase genes are pressed into services other than transposition. Transposons are central to the epigenetic phenomenon of “imprinting” that imbues genes with different expression patterns depending on whether they were transmitted through male or female gametes (Chapter 7), differences that arise during the major epigenetic reprogramming that takes place during gametogenesis (Chapter 5).

Although ideas about junk DNA have evolved substantially over the past two decades, the transposon monikers have stuck. Transposons are still referred to as “selfish” DNA, “invaders” and “parasites,” with the subtext that they are largely dangerous and destructive, hence in need of taming. The idea that epigenetic mechanisms evolved precisely to “control” the destructive potential of such “parasites,” advanced a decade and a half ago, has also persisted.

The value of these notions diminishes as we learn more about epigenetic mechanisms and gain insight into how transposons shape genomes. The real puzzle is that transposons accumulate in large numbers in eukaryotes, but not in prokaryotes. But this is also true of other categories of sequences, both coding and noncoding. That is, what distinguishes eukaryotic genome organization from that of prokaryotes is the ability to retain and manage large amounts of duplicated DNA. How did eukaryotes tip the balance between duplication and deletion that keeps genome size small in organisms in which homology-dependent recombination mechanisms predominate?

The answer to these questions lies precisely in the epigenetic mechanisms that eukaryotes have elaborated to a much greater extent than prokaryotes. Plants have a more complex and redundant array of epigenetic mechanisms even than animals (Chapter 5); importantly, however, transposons are not its only targets. A common denominator triggering silencing is the repetitive character of the sequence, not its identity as a transposon. Repeats are readily eliminated by unequal crossing over by homologous recombination and it is precisely homologous crossing over that is subject to increasingly stringent control in eukaryotic evolution.

The capacity to keep duplicated sequences is an essential step in the evolution of multicellular organisms, underpinning the ability to target expression of different subsets of genes to different cells and tissues. Equally key is the ability to program genes for differential expression by a variety of mechanisms, among which are the relatively stable mechanisms involving DNA and histone modification, as well as the more labile small-RNA-mediated mechanisms.

Because homology-dependent illegitimate recombination events between transposons in different locations have the potential to disrupt genomes, the very ability to suppress illegitimate recombination must inevitably favor the accumulation of transposons, the results of whose antics might otherwise be relegated to the evolutionary scrap heap. Thus it was perhaps the elaboration of epigenetic mechanisms originating in prokaryotes to moderate homologous recombination that made it possible for genomes to grow by duplication and for transposons to proliferate. This is precisely the inverse of the “parasite control” hypothesis, which posits that epigenetic mechanisms arose to control transposons.

And yet, even though epigenetic silencing mechanisms effectively minimize transposable element activity, they do not eliminate it, and the fingerprints of transposon activity are evident at every level of genome organization. That brings me to the final piece of the puzzle McClintock left us. McClintock described the suite of nuclear events, including transposon activation and various chromosome aberrations and rearrangements, that unfold in the wake of what she called genomic “shocks,” such as irradiation or mutagenesis, or, as in her experiments, the introduction of two broken chromosomes by a genetic cross. It has, by now, been amply documented that plant transposons are activated in response to a variety of genomic perturbations and both biotic and abiotic stresses, including pathogen infection, the passage of plant cells through tissue culture, interspecific hybridization and allopolyploidization (Chapters 2, 6, and 9). This appears to be true, as well, in other eukaryotes, from yeast to flies to humans, and the common denominator is, of course, DNA damage. Chapter 9 proposes that dysregulation of the epigenetic machinery underlies responses to such genomic shocks. Experimental evidence has just begun to emerge from the molecular study of hybrid dysgenesis in Drosophila. A deeper understanding of how the epigenetic regulatory systems are themselves modulated to facilitate damage control and restore genome integrity remains for future investigations to unravel.

In sum, then, the present volume provides a rich picture of the role that TEs have played in sculpting the genomic landscape of plants at multiple levels of organization and on time scales from the generational to the evolutionary. Given their abundance in most higher-eukaryotic genomes, the ancient origins of the DNA resecting enzymes that they encode, and the clear evidence of their impact on gene and genome structure and regulation, there seems little value in continuing to view them as “parasites.” As well, given the ubiquity and variety of epigenetic regulatory mechanisms, it seems increasingly implausible that they were invented to control TEs. On the contrary, it seems more probable that TEs proliferated and came to drive eukaryotic genome evolution because of and not despite epigenetic regulation. The present volume documents the many ways that transposons have contributed to the evolution of plant genes and genomes, arguably explaining their extraordinary plasticity – indeed, their very evolvability.

Finally, there are many questions to be addressed once we accept TEs as legitimate – indeed, dominant – inhabitants of the eukaryotic genome. The extraordinary size of many plant genomes suggests that the accumulation of vast numbers of TEs and other kinds of repetitive DNAs is tolerable. Whether the large and rapidly evolving blocks of retrotransposons actually confer a selective advantage is not known. How might the transposon landscape of chromosomes influence the stability and the participation of chromosomes in the mechanics of mitosis and meiosis? The observations that retrotransposon blocks are recombinationally inert and that disruptions in epigenetic regulation disrupt meiosis may well be hints that will lead us to a deeper understanding of the architecture and dynamics of contemporary genomes.

1   The Discovery of Transposition1

Nina V. Fedoroff

Introduction

The discovery of transposition can be dated quite precisely. Writing about the first case of an unstable mutation caused by insertion of the Dissociation (Ds) locus, which she had earlier identified and named for its ability to cause chromosome breakage and dissociation, McClintock observes: “At the time, I did not know that Ds could change its location. Realization of this did not enter my consciousness until late this spring, following the harvest of the greenhouse crop.” Inked corrections in McClintock’s hand on a typed manuscript, never published, from January of 1949 identify the spring as that of 1948 and the greenhouse crop as that of winter 1947–1948.

Studies on Variegation

Not surprisingly, the discovery of transposition is embedded in a larger context, both in McClintock’s work and in earlier studies on what were initially called “mutable” or “unstable” genes and “ever-sporting” plant varieties that exhibit variegation for flower and leaf color. While these studies did not lead directly to McClintock’s discovery of transposable elements in the sense that she was working with such materials, she was undoubtedly aware of the earlier work, particularly that of Emerson and Rhoades. Both of these maize geneticists had carried out systematic genetic studies on mutable genes in maize and contributed substantial insights into their nature and behavior. Thus, it is with the work of these authors that the discussion begins, although it is important to note as preamble even earlier mention in the literature of the peculiar behavior of mutable genes.

De Vries, for example, developed a general concept of “ever-sporting” varieties from studies in Antirrhinum (de Vries, 1905). He concluded that the inheritance of variegation and the occasional fully colored mutations or “sports” arising from them generally do not show what we now call Mendelian inheritance, although he did report instances of the inheritance of somatic mutations to full color. Correns, working with , and East and Hays, studying variegation in , similarly noted that somatic mutations from a variegated to a fully colored phenotype showed Mendelian inheritance. To set the stage, it is worthwhile reproducing a diagram from de Vries experiments on () (de Vries, 1905).