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Interchromosomal Communication Coordinates Intrinsically Stochastic Expression Between Alleles

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Science  07 Feb 2014:
Vol. 343, Issue 6171, pp. 661-665
DOI: 10.1126/science.1243039

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Stochasticity and Cell Fate

Stochastic mechanisms can diversify cell fates in nervous systems. In the Drosophila retina, the stochastic distribution of color-sensing photoreceptors is controlled by the random, On/Off expression of the Spineless transcriptional regulator. Johnston and Desplan (p. 661) found that each allele of spineless makes an intrinsically random expression choice controlled by an enhancer and two silencer DNA elements acting at long range. spineless alleles communicate between chromosomes using activating and repressing mechanisms to determine the frequency of expression and coordinate expression state. These findings suggest critical roles for intrinsically random expression decisions and interchromosomal communication in stochastic cell fate specification.

Abstract

Sensory systems use stochastic mechanisms to diversify neuronal subtypes. In the Drosophila eye, stochastic expression of the PAS-bHLH transcription factor Spineless (Ss) determines a random binary subtype choice in R7 photoreceptors. Here, we show that a stochastic, cell-autonomous decision to express ss is made intrinsically by each ss locus. Stochastic on or off expression of each ss allele is determined by combinatorial inputs from one enhancer and two silencers acting at long range. However, the two ss alleles also average their frequency of expression through up-regulatory and down-regulatory interallelic cross-talk. This inter- or intrachromosomal long-range regulation does not require endogenous ss chromosomal positioning or pairing. Therefore, although individual ss alleles make independent stochastic choices, interchromosomal communication coordinates expression state between alleles, ensuring that they are both expressed in the same random subset of R7s.

  • * Present address: Department of Biology, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218, USA.

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