A fundamental tenet of classical mendelian genetics is that allelic information is stably inherited from one generation to the next, resulting in predictable segregation patterns of differing alleles. Although several exceptions to this principle are known, all represent specialized cases that are mechanistically restricted to either a limited set of specific genes (for example mating type conversion in yeast) or specific types of alleles (for example alleles containing transposons or repeated sequences). Here we show 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 chromosomal genome of their parents but was present in previous generations. This previously undescribed process is shown to occur at all DNA sequence polymorphisms examined and therefore seems to be a general mechanism for extra-genomic inheritance of DNA sequence information. We postulate that these genetic restoration events are the result of a template-directed process that makes use of an ancestral RNA-sequence cache.

SummaryThe outer epidermal plant cell wall and cuticle play an important role in regulating both abiotic and biotic interactions between the plant and its environment. In addition to acting as a protective barrier that limits water loss, the effects of detrimental irradiation and invasion by pathogens, the epidermis also offers an interface that is inert to interactions between organs and ensures proper separation and expansion of organs at the growing points of the plant. Here, we describe the molecular cloning and characterization of HOTHEAD (HTH ), a gene required to limit cellular interactions between contacting epidermal cells durinḡ oral development. HTH is a member of a small gene family in Arabidopsis and encodes an enzyme related to a group of FAD-containing oxidoreductases that have been described in several other species. Characterization of 11 independently derived mutant alleles suggests that key amino acids are shared between these related groups of enzymes and identify a cluster of other functionally important residues that are highly conserved only within the Arabidopsis gene family. Our ®ndings add this new type of enzyme to a growing list of enzymes that have been shown to be involved in regulating post-genital organ fusion. Expression analysis of the HTH gene shows that it is expressed in all tissues tested, including roots, and is not epidermis-speci®c. Furthermore, the sequence data unequivocally show that none of the alleles isolated are epigenetic alleles as suggested by genetic behavior previously observed at this locus.

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