Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene

Abstract

The b gene of maize encodes a transcriptional activator of anthocyanin pigment biosynthetic genes. Certain b alleles undergo paramutation: a unidirectional, heritable alteration of one allele caused by the presence of another allele. B-I (intensely pigmented plant) is always changed to B' (weakly pigmented plant) in the B'/B-I heterozygote, such that all progeny receive the B' allele. The "new" B', which was B-I in the previous generation, is weakly pigmented and fully capable of changing another B-I allele into B'. It was not previously known whether paramutation is associated with altered b expression, altered B protein function or both. Our results show that B' acts in trans to suppress the transcription of B-I, with transcription remaining low in subsequent generations, even when the original B' allele segregates away. The products of B-I and B' are equally capable of activating the transcription of their target genes, indicating they are functionally equivalent. Genomic restriction maps, DNA sequence and methylation of B' and B-I were compared. Despite dramatic differences in phenotype and transcription of B' and B-I, no evidence for rearrangements, changes in sequence or changes in methylation was found. These results provide no support for models involving "dominant negative" proteins, gene conversion or transposable element interactions. We suggest that b paramutation involves a physical interaction between the alleles that suppresses transcription and promotes a change in chromatin structure that is heritable.