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For many genes, proper gene expression requires coordinated and dynamic interactions between multiple regulatory elements, each of which can either promote or silence transcription. In  Drosophila , the complexity of the regulatory landscape is further complicated by the tight physical pairing of homologous chromosomes, which can permit regulatory elements to interact in  trans , a phenomenon known as transvection. To better understand how gene expression can be programmed through  cis-  and  trans- regulatory interactions, we analyzed transvection effects for a collection of alleles of the  eyes absent  ( eya ) gene. We find that  trans -activation of a promoter by the  eya  eye-specific enhancers is broadly supported in many allelic backgrounds, and that the availability of an enhancer to act in  trans  can be predicted based on the molecular lesion of an  eya  allele. Furthermore, by manipulating promoter availability in  cis  and in  trans , we demonstrate that the eye-specific enhancers of  eya  show plasticity in their promoter preference between two different transcriptional start sites, which depends on promoter competition between the two potential targets. Finally, we show that certain alleles of  eya  demonstrate pairing-sensitive silencing resulting from  trans -interactions between Polycomb Response Elements (PREs), and genetic and genomic data support a general role for PcG proteins in mediating transcriptional silencing at  eya . Overall, our data highlight how  eya  gene regulation relies upon a complex but plastic interplay between multiple enhancers, promoters, and PREs.

Two modes of transvection at the eyes absent gene of Drosophila demonstrate plasticity in transcriptional regulatory interactions in cis and in trans