Genome communication

June 30, 2008

Alleles of homologous genes can silence one another through paramutations

In the late 19th century Gregor Mendel used peas to show that one copy of a gene (allele) is inherited from the mother and one from the father. In the progeny, the inherited genes are expressed at the right time and in the right place, but until recently, it was thought that although gene products could be modified during the life of the organism, the genes themselves were unchanged, except for random mutation. Now it appears that one copy of some genes can alter the expression of the other copy, and those changes are passed down to the next generation. These epigenetic alterations, called paramutations may be important in introducing changes when plants and other organisms are environmentally stressed. The exact mechanisms of how genes talk to other genes and change their behavior are being investigated, and recent results suggest that these processes could be important in engineering plants responsive to a variety of environmental conditions.

Dr. Vicki Chandler and her colleagues have studied paramutations in maize and other plants and have identified some of the genes and mechanisms that operate in this epigenetic process. Dr. Chandler, of the Department of Plant Sciences at the University of Arizona, Tucson, will be presenting this work at a symposium on Maize Biology at the annual meeting of the American Society of Plant Biologists in Mérida, Mexico (June 28, 9:10 AM).

The sequencing of genes, proteins, and, ultimately, whole genomes has revealed that genomes are not simply strings of genes, but rather complex, communicating, and interacting regions of information that could be compared to DNA computers controlling growth, development, and metabolism in each organism. The physical architecture of the genome is also highly complex. The nucleus, where the genome resides, is not full of strings of DNA like a pot of spaghetti. Rather, the strands of DNA are wrapped around proteins called histones and the whole is organized into an elegant and highly controlled structure called chromatin. When it is time for genes to be expressed, a section of chromatin is unwound and the DNA for that particular gene is made available to the machinery that transcribes DNA to RNA. Once the process is finished, the DNA is neatly folded back into the chromatin structure until needed again. Different parts of the genome can interact by direct contact or through intermediaries that can be proteins or RNA sequences. The exact mechanisms of how paramutagenic alleles communicate with their homologous partners are still unknown, but the work of Chandler and others suggests that both direct contact of homologous regions and changes induced by intermediary RNA molecules may be involved.

Peas also played an important role in the discovery of paramutations, as the first mutants of this type were observed in peas in 1915. Then, in the 1950s, Alexander Brink identified these types of mutations as interactions between alleles. He recognized that these interactions resulted in heritable changes to the expression of those genes. Since then, paramutations have been found in humans and other animals, as well as other plant species including tomato, tobacco, petunia, and maize. In animals, paramutations may be important in mediating the occurrence of diseases like diabetes. Chandler and her co-workers have been investigating paramutations in maize at the b1 gene, which regulates the distribution of the purple pigment anthocyanin in plant tissues.

At the b1 locus, the paramutagenic allele, which causes light or stippled pigmentation arises spontaneously from the wild-type allele, which causes dark purple pigmentation. If a plant with the paramutagenic allele is crossed with a wild-type allele, the progeny get both alleles. However, the paramutagenic allele silences the wild-type allele and produces a plant with stippled rather than purple pigmentation. The silent state is then passed on in subsequent crosses.

Several different components may be involved in paramutation, although they may differ among species. One important player is an array of repeated non-coding DNA sequences that lies upstream of the gene sequence of the paramutagenic allele. Seven of these tandem repeats are required for b1 paramutation. If only three tandem repeats are present, there is only partial paramutagenic activity. One possibility is that these tandem repeats are involved in direct interactions of chromatin regions, which results in paramutation changes. However, RNA also appears to be part of the process. The gene mediator of paramutation1 (mop1), an RNA dependent RNA polymerase is absolutely required for paramutation silencing at the b1 locus as well as for several other maize genes. In Arabidopsis, this RNA polymerase is associated with the production of small, interfering RNAs (siRNA) that function in gene silencing in other contexts. The siRNA could thus act as an intermediary molecule, being sent to silence the homologous allele. A third component is the placement of methyl groups on the control sequence (promoter) of the wild-type gene. Gene methylation has been known for some time as a cell defense mechanism for silencing foreign DNA but is also functional in other cellular processes. In several species, such methylation is also directed by RNA molecules. None of these processes is likely to be sufficient by themselves to effect paramutation, but rather all of them may interact, although to varying degrees in different species.

The molecular components of paramutation probably arose as cell defense mechanisms against viral or bacterial DNA. They have evolved to serve the needs of plants that grow in complex and changing environments from which they cannot escape, but to which they may be able to adapt through mechanisms like paramutation. Indeed, two instances of paramutation are known to be influenced by temperature. This work has implications for engineering crops that may be able to adapt to higher temperatures or drought conditions, as well as for applications in human and veterinary medicine.

American Society of Plant Biologists

PARAMUTATION AND CHROMOSOME ORGANIZATION
by R.A. Brink (Author)

Annual Plant Reviews, Plant Epigenetics (Volume 19)
by Peter Meyer (Editor)

With the discovery of RNAi pathways and the histone code, epigenetics has become a popular and fast evolving research topic. Plant science has made a number of elementary contributions to this field, and the common elements of epigenetic systems have linked research groups interested in plant, fungal and animal systems.

This volume provides a comprehensive overview epigenetic mechanisms and biological processes in plants, illustrating the wider relevance of this research to work in other plant science areas and on non-plant systems. It discusses recent advances in our knowledge of basic mechanisms and molecular components that control transcriptional and post-transcriptional silencing, an understanding of which is essential for plant researchers who use transgenic lines for...

Plant Gene Silencing
by M.A. Matzke (Editor), A.J.M. Matzke (Editor)

This book is an up-to-date and comprehensive collection of reviews on various aspects of epigenetic gene silencing in plants. Research on this topic has undergone explosive growth during the past decade and has revealed novel features of gene regulation and plant defense responses that also apply to animals and fungi. Gene silencing is relevant for agricultural biotechnology because stable expression of transgenes is required for the successful commercialization of genetically engineered crops. The reviews have been written by distinguished authors who have made significant contributions to plant gene silencing research. This volume supersedes other books on gene silencing by focussing on plant systems, where many pioneering experiments have been performed, and by including the...

Epigenetics: Cold Spring Harbor Symposia on Quantitative Biology, Volume LXIX
by Bruce Stillman (Editor)

The importance of epigenetic regulation of gene expression, particularly in higher organisms, is now clear and the 2004 Cold Spring Harbor Annual Symposium provided many new examples as well as insights into the underlying mechanisms. The resulting volume with over 60 papers from experts across the field covers various aspects of nuclear organization and dynamics; genomic imprinting, chromosomal inactivation, and other examples of gene silencing; the histone and DNA modifications associated with these conditions; and the roles of RNA and protein regulators in establishing and maintaining these states. The paperback version does not offer online access.

Handbook of Epigenetics: The New Molecular and Medical Genetics
by Trygve Tollefsbol (Editor)

Epigenetics is considered by many to be the "new genetics" because the realization that many biological phenomena are controlled not through gene mutations, but rather through reversible and heritable epigenetic processes that have opened up new paths for discovery. The biological processes impacted by epigenetics range from tissue/organ regeneration, X-chromosome inactivation, and stem cell differentiation to genomic imprinting and aging. The effects of epigenetics are vast and encompass lower organisms as well as humans. Aberrations of epigenetics influence many diseases involving but not limited to cancer, immune disorders, neurological and metabolic disorders, and imprinting diseases. Clinical intervention is already in place for some of these disorders and many novel epigenetic...

Epigenomics
by Anne C. Ferguson-Smith (Editor), John M. Greally Ph.D. (Editor), Rob A. Martienssen (Editor)

Epigenetic modifications act on DNA and its packaging proteins, the histones, to regulate genome function. Manifest as the heritable methylation of DNA and as post-translational histone modifications, these molecular flags influence the architecture and integrity of the chromosome, the accessibility of DNA to gene regulatory components and the ability of chromatin to interact within nuclear complexes. While a multicellular individual has only one genome, it has multiple epigenomes reflecting the diversity of cell types and their properties at different times of life; in health and in disease. Relationships are emerging between the underlying DNA sequence and dynamic epigenetic states and their consequences,such as the role of RNA interference and non-coding RNA. These integrated...

Advances in Agronomy, Volume 100
by Donald L. Sparks (Series Editor)

Contributors to this special 100th volume were carefully selected by the editor for their perspectives on not only the current state-of-the-art of their topic but also where their fields are going and what future opportunities exist to advance scientific frontiers. Originating in 1949, Advances in Agronomy is a venerable serial review featuring state-of-the-art reviews on crop and soil sciences over the years, and is highly regarded around the world. Volume 100 continues this long tradition of excellence, with cutting-edge and visionary reviews from distinguished scientists at the top of their respective fields.

* Contributions from leading scientists in crop and soil sciences and allied fields including geochemistry, environmental...

Transformations of Lamarckism: From Subtle Fluids to Molecular Biology (Vienna Series in Theoretical Biology)
by Snait B. Gissis (Editor), Eva Jablonka (Editor), Anna Zeligowski (Editor)

In 1809--the year of Charles Darwin's birth--Jean-Baptiste Lamarck published Philosophie zoologique, the first comprehensive and systematic theory of biological evolution. The Lamarckian approach emphasizes the generation of developmental variations; Darwinism stresses selection. Lamarck's ideas were eventually eclipsed by Darwinian concepts, especially after the emergence of the Modern Synthesis in the twentieth century. The different approaches--which can be seen as complementary rather than mutually exclusive--have important implications for the kinds of questions biologists ask and for the type of research they conduct. Lamarckism has been evolving--or, in...

Plant Breeding Reviews (Volume 30)
by Jules Janick (Editor)

Plant Breeding Reviews presents state-of-the-art reviews on plant breeding and genetics covering horticultural, agronomic and forestry crops, incorporating both traditional and molecular methods. The contributions are authored by world authorities, anonymously reviewed, and edited by Professor Jules Janick of Perdue University, USA. The series is an indispensible resource for crop breeders, plant scientists, and teachers involved in crop improvement and genetic resources. Initiated in 1983, Plant Breeding Reviews is published in the form of one or two volumes per year.Recently published articles include:Epigenetics and Plant Breeding (v30) Enhancing Crop Gene Pools with Beneficial Traits Using Wild Relatives (v30) Coffee Germplasm Resources, Genomics and Breeding (v30) Molecular...

Maize Genetics and Breeding in the 20th Century
by Peter A. Peterson (Editor), Angelo Bianchi (Editor)

This book provides biographics and a related summary of geneticists and breeders of maize that were contributors to the major discoveries in the 20th century. Their relationships to each other, as well as general developments in maize genetics and breeding growth, are included. Photos of events and related personnel, all part of the bibliographic presentation, present a compilation of the maize community and its growth. Most of the geneticists and breeders have a common origin in training and their progeny are part of the current contributors to maize development.