Paramutation is the ability of specific DNA sequences to communicate in trans to establish meiotically heritable expression states. Paramutation at the maize b1 locus is mediated by seven unique noncoding transcribed tandem repeats of 853 bp that are required to establish and maintain the meiotically heritable expression and distinct chromatin states associated with b1 paramutation. In this study, we report the identification of a CXC-domain protein CBBP (CXC domain b1-repeat binding protein) that binds to a defined region within the b1 tandem repeat sequence in vivo and in vitro. When CBBP is expressed from a transgene in maize, it can induce a silent state at the b1 locus that is heritable in progeny no longer containing the transgene, and the silent epiallele is capable of silencing an active epiallele, characteristic of paramutation. Accumulation of the CBBP protein correlates with b1 silencing in transgenic and nontransgenic plants. The ability of CBBP to form multimers and to bind to the b1 tandem repeats suggests a model for counting the number of b1 repeats. In contrast to previously identified proteins involved in paramutation, CBBP does not share similarity to the known components of the Arabidopsis RNAi heterochromatin silencing pathway. Thus, this study defines another class of protein that is involved in heritable gene silencing.chromatin | gene silencing P aramutation was initially described at the maize r1 locus (1) as an interaction between specific alleles that leads to heritable changes in expression. Since that time, several other examples of paramutation were identified in maize and in other species, including other plants, fungi, and animals (see refs. 2-5 for review). Recent findings demonstrated an essential role for RNAi in paramutation, as four cloned genes involved in paramutation encode proteins closely related to RNAi pathway components (6-9).Herein we focus on paramutation at b1, a locus that encodes a transcription factor required to activate the purple anthocyanin pigment biosynthetic pathway. Two epialleles that participate in paramutation, B-I and B′, have the same DNA sequences (10) but distinct epigenetic states (11). B-I has a high transcription rate, resulting in homozygous dark purple plants, whereas B′ plants are lightly pigmented because of a reduced transcription rate. In heterozygous plants, B-I is always changed (paramutated) to B′. The new B′ epiallele is fully capable of paramutating naïve B-I epialleles in subsequent generations (11). The B′ epiallele is extremely stable; changes from B′ to B-I have never been observed in wild-type genetic backgrounds. In contrast, B-I is unstable and can spontaneously change to B′ at variable frequencies of 0.1-10% (11, 12).The key sequences required for b1 paramutation are seven unique tandem repeats of an 853-bp noncoding DNA located ∼100 kb upstream of the b1 transcription start site (10). Although this sequence and the number of repeats are identical in B-I and B′ epialleles, the DNA methylation pattern and chromatin structure d...
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