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Taxon-specific, phased siRNAs underlie a speciation locus in monkeyflowers

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Taxon-specific small RNA loci are widespread in eukaryotic genomes, yet their role in lineage-specific adaptation, phenotypic diversification, and speciation is poorly understood. Here, we report that a speciation locus in… Click to show full abstract

Taxon-specific small RNA loci are widespread in eukaryotic genomes, yet their role in lineage-specific adaptation, phenotypic diversification, and speciation is poorly understood. Here, we report that a speciation locus in monkeyflowers (Mimulus), YELLOW UPPER (YUP), contains an inverted repeat region that produces small interfering RNAs (siRNAs) in a phased pattern. Although the inverted repeat is derived from a partial duplication of a protein-coding gene that is not involved in flower pigmentation, one of the siRNAs targets and represses a master regulator of floral carotenoid pigmentation. YUP emerged with two protein-coding genes that control other aspects of flower coloration as a “superlocus” in a subclade of Mimulus and has contributed to subsequent phenotypic diversification and pollinator-mediated speciation in the descendant species. Description Noncoding gene drives floral speciation In monkeyflowers (Mimulus spp.), variation in the YELLOW UPPER (YUP) genetic locus causes changes in flower color patterns that in turn drive speciation with shifts in whether the flower is pollinated by bees or by hummingbirds. Liang et al. show that the locus does not encode a protein (see the Perspective by Monniaux). Instead, YUP produces phased small interfering RNAs that regulate floral carotenoid pigmentation. Revealing the opportunistic nature of evolution, the locus evolved from a fragment of a gene encoding a cytochrome protein not involved in floral pigment production. —PJH A genetic locus–involved Mimulus speciation encodes a set of small regulatory RNAs.

Keywords: locus; taxon specific; specific phased; locus monkeyflowers; speciation; speciation locus

Journal Title: Science
Year Published: 2023

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