Genome-wide non-mendelian inheritance
Genome-wide non-mendelian inheritance of extra-genomic information: at the cross-road of a paradigmatic shift ?
Achigan-Dako G.E.(1), Gaoue O.G.(2)
1 Institute of Plant Genetics and Plant Crops Research, D-06466 Gatersleben, Germany. email. dachigan@yahoo.fr (Author for correspondence)
² University of Hawaii at Manoa, Botany Dept. 3190 Maile Way, 101. Honolulu, HI 96822 USA. ogaoue@hawaii.edu
Heredity is the cornerstone for genetics. But recent developments in genetics say epigenetics (coined expression to design phenomena that lead to changes in gene function that are mitotically and/or meiotically transmissible without entailing a change in DNA sequence) seem to withdraw from genetics it primary object: the heredity. It is true that genes have played biology's centre stages for decades. But whereas the genes always seem to get star billing, works over the past few years suggest that they are little more than puppets (Pennisi 2001). The implications of these thoughts relay in the multiples questions stated by van de Vijver (2002): does epigenetics challenge traditional insights in genetics, development and evolution? Is it prefiguring, from within biology, the end of a common ground, that is, the gene as master molecule symbolised in molecular biology central dogma? Does it challenge the idea that genes code for the essential characteristics of life?
Recent work of Lolle et al. (2005) brought new insights and new answers through what we could call a discovery of genome-wide non-mendelian inheritance of extra-chromosomal information. They showed that Arabidopsis plants homozygous for recessive mutant alleles of the organ fusion gene HOTHEAD (HTH) can inherit allele specific DNA sequence information that was not present in the immediate parent chromosomal genome but rather present in the grandparent's genome. These mutant parents certainly have hidden templates containing the information that leads to the reversion of the HTH allele. Through the several experiments that they carried out it was clear that the inheritance process showed by this widely used plant does not follow the mendelian law and the conventional known process. Even though the frequency of such an event could be very low in the nature it is important to wonder what role this process play in the whole evolutionary process and at what extent it happens.
Through the new developments of genetic works we should be more aware that behind the scenes of gene expression (Pennisi 2001) and the environmental effects there is an additional hereditary function devoted not to the genes but to the non-gene. Consequently one could say that the genes are not the main maker of a character but are simply a "worker" in the transcriptional process. The sequence reversion observed by Lolle et al. (2005) is restricted nor to the DNA neither to the messenger RNA which should have been an obvious candidate to explain this mysterious reversion (Weigel and Jürgens 2005). Hence the hth "allele healer gene" seems to apply globally to other sequences in the genome and its locations is in the exon (coding region) but also in the intron (non-coding region) and in the 3'untranscriptional region of those gene. Although the mechanism of such a phenomenon is still mysterious, it might have oriented many mutation processes and insured the conservation of the original genome in plant and animal. And with a certain confidence one could say that it is no longer sufficient to restrict research to classical genetic analysis in terms of genetic mutations, distinct phenotypes-genotypes distinctions, and metaphors of genetic programs (van de Vijver 2002).
The findings of Lolle et al. (2005) brought out important lessons. The very first is the definition of gene and its hereditary function. In a simple Mendelian study recessive individuals homozygote for a genotype could never produce heterozygote individuals. But in Arabidopsis individuals recessive for the HOTHEAD gene it does happen; and moreover the dominant allele is far to originate from the DNA but completely outside DNA sequence. In consequence the Mendel's law is not absolute and here come then back on top of the surface the questions stated a couple of years ago by Bacon in Wu and Morris (2001): is there no doubt that gene can be simply defined as a single chemical, the deoxyribonucleic acid, or DNA? Shouldn't we go back to the Wilhem's view of the gene who regards it from the standpoint of its consequences on inheritance? Works on Arabidopsis provided answers that heredity is not always under DNA control, and if genes are responsible for variation and heredity, then genes are not equal to DNA. In consequence talking about genes should not be restricted to the DNA and its transcriptional function that involve mRNA. Rather scientists, particularly geneticists, at this cross-road of paradigms should extend their view about what a gene in a living organism is and should not restrict themselves to chemicals or isolable things (Wu and Morris 2001). All of inheritance cannot lie neatly at the feet of four nitrogenous bases.
The second lesson we learned from Lolle et al. (2005) is related to the dynamic and organizational strategy in living systems. Here we share the viewpoint of van de Vijver et al (2002) and the general theory of complexly organized dynamic systems, in which the mechanisms, the means, and the modalities by which such systems generate, organize, reorganize and sustain their relative stability and autonomy at various time-scale is set out (Collier and Hooker 1999). This opens a room to revisit concepts and theories in evolution where the whole story is based on the equation: gene mutation in a population given a particular environment and through spurts or gradual change, equal new individuals other new species when isolating barriers may act together to prevent gene flow. But how the non-DNA (Wu and Morris 2001) interacts with the environment to monitor new changes has been for long left out. If in the evolution process genes are followers, not the leaders (West-Eberhard 2003) we should also be flexible and not to consider in the sense of Rollo (2004) that there can be no initial phenotype without a genotype and no evolution without selection that alter the genome, including heritable changes in chromatin structure). This heritability through genes is actually problematic even though mechanisms for the process to happen are still mysterious. Maybe shouldn't we look at genes as a DNA molecules but rather as virtual objects that govern heredity and variation. Exquisite precision in the timing of gene expression should not be taken as evidence for the genetic orchestration of development. The predictable effects of genes depend as much on the specific organized flexibility, modular differentiation and local conditions within a pre-existing structure as they do on the specificity of the genes themselves (West-Eberhard 2003).
The capacity of a species to consider its situation, to evaluate its logistics of survival and to self-organize both continuity and morphological versions of type (Maze et al. 2005) should not be devoted to chromosomes only. Chromosomes are simple agents of the cell which may not possess the developmental and evolutionary history folder of the whole individual. Should we then continue with the dogma on DNA and its supremacy on the heredity or should we learn on the mysterious work of nature that allow structure to form de novo from the apparent structureless mass that results from the union of egg and sperm (Wu and Morris 2001)? Whatever it is the cell or the individual or why not the species deals with a mode of organization of information, embedded not as propensities of a singular morphology type but as a link with other propensities within and outside any morphological type. Maze et al. (2005) coined such organization mode as the "virtual mode" which is a complex provisor of information that includes real propensities such as genes, sets of genes, and imaginary propensities still unknown. Without this complex mode the species must base its adaptive function only on the random mechanical process of accidental misreading of the genes. Fortunately, over the genes, the DNA molecule, exists what Lolle et al. (2005) desperately called the template-cache where information can be found to mysteriously produce gene reversion defying Mendel's inheritance law. How can we isolate this mysterious ''hand''? Or should we refer to the natural theology of the 18th century?
References
Collier J, Hooker C. 1999. Complexly organised dynamical systems. Open Systems Information dynamic 6: 241-302.
Lolle SL, Victor JL, Young MJ, Pruit RE. 2005. Genome-wide non medelian inheritance of extra-chromosomic information in Arabidopsis. Nature 434: 505-509.
Maze J, Taborsky E, Finnegan CV. 2005. The virtual mode: a different look at species. Taxon 54 (1): 131-132.
Pennisi E. 2001. Behind the scenes of genes expression. Science 293:1064-1075.
Rollo D. 2004. Life = epigenetics, ecology and evolution (L= E³): a review of developmental plasticity and evolution, by Mary Jane West Eberhard. Evolution & Development 6:1, 58-62.
van de Vijver G, van Speybroeck L, de Waele D. 2002. Epigenetics: a challenge for genetics, evolutions and development. Annals of New York Academy of Science 981:1-6.
Weigel D, Jürgens G. 2005. Hotheaded healer. Nature 434: 505-509.
West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford university Press. New york. 794 p.
Wu C-t, Morris JR. Genes, genetics and epigenetics: a correspondence. Sciencce 293: 1103-1105.
Achigan-Dako G.E.(1), Gaoue O.G.(2)
1 Institute of Plant Genetics and Plant Crops Research, D-06466 Gatersleben, Germany. email. dachigan@yahoo.fr (Author for correspondence)
² University of Hawaii at Manoa, Botany Dept. 3190 Maile Way, 101. Honolulu, HI 96822 USA. ogaoue@hawaii.edu
Heredity is the cornerstone for genetics. But recent developments in genetics say epigenetics (coined expression to design phenomena that lead to changes in gene function that are mitotically and/or meiotically transmissible without entailing a change in DNA sequence) seem to withdraw from genetics it primary object: the heredity. It is true that genes have played biology's centre stages for decades. But whereas the genes always seem to get star billing, works over the past few years suggest that they are little more than puppets (Pennisi 2001). The implications of these thoughts relay in the multiples questions stated by van de Vijver (2002): does epigenetics challenge traditional insights in genetics, development and evolution? Is it prefiguring, from within biology, the end of a common ground, that is, the gene as master molecule symbolised in molecular biology central dogma? Does it challenge the idea that genes code for the essential characteristics of life?
Recent work of Lolle et al. (2005) brought new insights and new answers through what we could call a discovery of genome-wide non-mendelian inheritance of extra-chromosomal information. They showed that Arabidopsis plants homozygous for recessive mutant alleles of the organ fusion gene HOTHEAD (HTH) can inherit allele specific DNA sequence information that was not present in the immediate parent chromosomal genome but rather present in the grandparent's genome. These mutant parents certainly have hidden templates containing the information that leads to the reversion of the HTH allele. Through the several experiments that they carried out it was clear that the inheritance process showed by this widely used plant does not follow the mendelian law and the conventional known process. Even though the frequency of such an event could be very low in the nature it is important to wonder what role this process play in the whole evolutionary process and at what extent it happens.
Through the new developments of genetic works we should be more aware that behind the scenes of gene expression (Pennisi 2001) and the environmental effects there is an additional hereditary function devoted not to the genes but to the non-gene. Consequently one could say that the genes are not the main maker of a character but are simply a "worker" in the transcriptional process. The sequence reversion observed by Lolle et al. (2005) is restricted nor to the DNA neither to the messenger RNA which should have been an obvious candidate to explain this mysterious reversion (Weigel and Jürgens 2005). Hence the hth "allele healer gene" seems to apply globally to other sequences in the genome and its locations is in the exon (coding region) but also in the intron (non-coding region) and in the 3'untranscriptional region of those gene. Although the mechanism of such a phenomenon is still mysterious, it might have oriented many mutation processes and insured the conservation of the original genome in plant and animal. And with a certain confidence one could say that it is no longer sufficient to restrict research to classical genetic analysis in terms of genetic mutations, distinct phenotypes-genotypes distinctions, and metaphors of genetic programs (van de Vijver 2002).
The findings of Lolle et al. (2005) brought out important lessons. The very first is the definition of gene and its hereditary function. In a simple Mendelian study recessive individuals homozygote for a genotype could never produce heterozygote individuals. But in Arabidopsis individuals recessive for the HOTHEAD gene it does happen; and moreover the dominant allele is far to originate from the DNA but completely outside DNA sequence. In consequence the Mendel's law is not absolute and here come then back on top of the surface the questions stated a couple of years ago by Bacon in Wu and Morris (2001): is there no doubt that gene can be simply defined as a single chemical, the deoxyribonucleic acid, or DNA? Shouldn't we go back to the Wilhem's view of the gene who regards it from the standpoint of its consequences on inheritance? Works on Arabidopsis provided answers that heredity is not always under DNA control, and if genes are responsible for variation and heredity, then genes are not equal to DNA. In consequence talking about genes should not be restricted to the DNA and its transcriptional function that involve mRNA. Rather scientists, particularly geneticists, at this cross-road of paradigms should extend their view about what a gene in a living organism is and should not restrict themselves to chemicals or isolable things (Wu and Morris 2001). All of inheritance cannot lie neatly at the feet of four nitrogenous bases.
The second lesson we learned from Lolle et al. (2005) is related to the dynamic and organizational strategy in living systems. Here we share the viewpoint of van de Vijver et al (2002) and the general theory of complexly organized dynamic systems, in which the mechanisms, the means, and the modalities by which such systems generate, organize, reorganize and sustain their relative stability and autonomy at various time-scale is set out (Collier and Hooker 1999). This opens a room to revisit concepts and theories in evolution where the whole story is based on the equation: gene mutation in a population given a particular environment and through spurts or gradual change, equal new individuals other new species when isolating barriers may act together to prevent gene flow. But how the non-DNA (Wu and Morris 2001) interacts with the environment to monitor new changes has been for long left out. If in the evolution process genes are followers, not the leaders (West-Eberhard 2003) we should also be flexible and not to consider in the sense of Rollo (2004) that there can be no initial phenotype without a genotype and no evolution without selection that alter the genome, including heritable changes in chromatin structure). This heritability through genes is actually problematic even though mechanisms for the process to happen are still mysterious. Maybe shouldn't we look at genes as a DNA molecules but rather as virtual objects that govern heredity and variation. Exquisite precision in the timing of gene expression should not be taken as evidence for the genetic orchestration of development. The predictable effects of genes depend as much on the specific organized flexibility, modular differentiation and local conditions within a pre-existing structure as they do on the specificity of the genes themselves (West-Eberhard 2003).
The capacity of a species to consider its situation, to evaluate its logistics of survival and to self-organize both continuity and morphological versions of type (Maze et al. 2005) should not be devoted to chromosomes only. Chromosomes are simple agents of the cell which may not possess the developmental and evolutionary history folder of the whole individual. Should we then continue with the dogma on DNA and its supremacy on the heredity or should we learn on the mysterious work of nature that allow structure to form de novo from the apparent structureless mass that results from the union of egg and sperm (Wu and Morris 2001)? Whatever it is the cell or the individual or why not the species deals with a mode of organization of information, embedded not as propensities of a singular morphology type but as a link with other propensities within and outside any morphological type. Maze et al. (2005) coined such organization mode as the "virtual mode" which is a complex provisor of information that includes real propensities such as genes, sets of genes, and imaginary propensities still unknown. Without this complex mode the species must base its adaptive function only on the random mechanical process of accidental misreading of the genes. Fortunately, over the genes, the DNA molecule, exists what Lolle et al. (2005) desperately called the template-cache where information can be found to mysteriously produce gene reversion defying Mendel's inheritance law. How can we isolate this mysterious ''hand''? Or should we refer to the natural theology of the 18th century?
References
Collier J, Hooker C. 1999. Complexly organised dynamical systems. Open Systems Information dynamic 6: 241-302.
Lolle SL, Victor JL, Young MJ, Pruit RE. 2005. Genome-wide non medelian inheritance of extra-chromosomic information in Arabidopsis. Nature 434: 505-509.
Maze J, Taborsky E, Finnegan CV. 2005. The virtual mode: a different look at species. Taxon 54 (1): 131-132.
Pennisi E. 2001. Behind the scenes of genes expression. Science 293:1064-1075.
Rollo D. 2004. Life = epigenetics, ecology and evolution (L= E³): a review of developmental plasticity and evolution, by Mary Jane West Eberhard. Evolution & Development 6:1, 58-62.
van de Vijver G, van Speybroeck L, de Waele D. 2002. Epigenetics: a challenge for genetics, evolutions and development. Annals of New York Academy of Science 981:1-6.
Weigel D, Jürgens G. 2005. Hotheaded healer. Nature 434: 505-509.
West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford university Press. New york. 794 p.
Wu C-t, Morris JR. Genes, genetics and epigenetics: a correspondence. Sciencce 293: 1103-1105.

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