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A Stop-Gain Mutation Within MLPH Is Responsible for the Lilac Dilution Observed in Jacob Sheep

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A Stop-Gain Mutation Within MLPH Is Responsible for the Lilac Dilution Observed in Jacob Sheep G C A T T A C G G C A T genes Communication A Stop-Gain Mutation within MLPH Is Responsible for the Lilac Dilution Observed in Jacob Sheep Christian J. Posbergh 1,* , Elizabeth A. Staiger 1,2 and Heather J. Huson 1,* 1 Department of Animal Science, Cornell University, Ithaca, NY 14853, USA; [email protected] 2 Department of Animal Sciences, Auburn University, Auburn, AL 36849, USA * Correspondence: [email protected] (C.J.P.); [email protected] (H.J.H.) Received: 7 May 2020; Accepted: 2 June 2020; Published: 4 June 2020 Abstract: A coat color dilution, called lilac, was observed within the Jacob sheep breed. This dilution results in sheep appearing gray, where black would normally occur. Pedigree analysis suggested an autosomal recessive inheritance. Whole-genome sequencing of a dilute case, a known carrier, and sixteen non-dilute sheep was used to identify the molecular variant responsible for the coat color change. Through investigation of the genes MLPH, MYO5A, and RAB27A, we discovered a nonsynonymous mutation within MLPH, which appeared to match the reported autosomal recessive nature of the lilac dilution. This mutation (NC_019458.2:g.3451931C>A) results in a premature stop codon being introduced early in the protein (NP_001139743.1:p.Glu14*), likely losing its function. Validation testing of additional lilac Jacob sheep and known carriers, unrelated to the original case, showed a complete concordance between the mutation and the dilution. This stop-gain mutation is likely the causative mutation for dilution within Jacob sheep. Keywords: Ovis aries; coat color; whole-genome sequencing; genomics 1. Introduction Coat color is suspected to be one of the first traits selected for in livestock species after domestication. Historically, selection in sheep has been for white wool, due to its ability to be dyed, as opposed to nonwhite wool. While white wool remains the dominant product in the commercial wool market, nonwhite wool can bring higher prices in niche markets. Nonwhite wool comes in a variety of patterns and colors, which breeders can select to increase the revenue from wool sales. One such nonwhite coat color variation is dilution, which is commonly represented by lighter shades of color pigmentation. A dilute phenotype has been observed within the Jacob breed, often called lilac. This dilution results in the nonwhite portions of the wool appearing gray, rather than the traditional black. Based on pedigree analysis of the Jacob Sheep Breeders Association registry, the dilution is inherited and expressed in an autosomal recessive pattern [1]. Dilute coat color phenotypes are commonly the result of impaired melanosome transport, leading to an irregular clustering of pigment. This irregular clustering of melanosomes results in decreased light absorption in the fiber, resulting in black hair or wool that appears grey. Melanophilin, together with myosin Va and Rab27a, form a protein complex that is responsible for transporting melanosomes to the cytoskeleton of melanocytes [2]. This complex has been shown to be required for proper melanosome transport [3]. Defects in any of these three genes, melanophilin (MLPH), myosin Va (MYO5A), and Rab27a (RAB27A), have been linked with several dilute phenotypes and the autosomal recessive Griscelli syndromes in humans (OMIM #214450, 607624, 609227) [4,5]. Of the Griscelli syndromes, type 3 (OMIM #609227) is linked to mutations within MLPH and is the only one of the three types to exhibit hypopigmentation in the absence of neurological or immunological abnormalities [5]. Genes 2020, 11, 618; doi:10.3390/genes11060618 www.mdpi.com/journal/genes Genes 2020, 11, x FOR PEER REVIEW 2 of 8 Genes 2020, 11, 618 2 of 8 Until now, no dilute phenotypes in sheep or goats have been associated with any specific molecular variants. Dilute phenotypes observed in chickens (OMIA #001445-9031) [6], dogs (OMIA Until now, no dilute phenotypes in sheep or goats have been associated with any specific molecular #000031-9615) [7–9], rabbits (OMIA #000031-9986) [10–12], cats (OMIA #000031-9685) [13], American variants. Dilute phenotypes observed in chickens (OMIA #001445-9031) [6], dogs (OMIA #000031-9615) [7–9], minks (000031-452646) [14,15], and Belgian Blue cattle (OMIA #000031-9913) [16] have all been linked rabbits(OMIA#000031-9986)[10–12], cats(OMIA#000031-9685)[13], Americanminks(000031-452646)[14,15], to variants within the melanophilin gene (MLPH). Therefore, MLPH was the most promising candidateand Belgian gene Blue to cattleinvestigate (OMIA for #000031-9913) variants contribu [16] haveting allto beenthe dilute linked phenotype to variants in within Jacob thesheep. melanophilin The purposegene (MLPH of this). Therefore,study was toMLPH identifywas the the genomic most promising variant(s) candidateresponsible gene for the to investigatelilac color seen for variantsin Jacobcontributing sheep, using to the dilutewhole-genome phenotype sequencing in Jacob sheep. and a The candidate purpose gene of this approach. study was By to utilizing identify whole- the genomic genomevariant(s) sequencing responsible of for a the known lilac color dilute seen case in Jacob and sheep,a known using carrier, whole-genome a premature sequencing stop-gain and apoint candidate mutationgene approach. was identified By utilizing within whole-genome MLPH. This work sequencing adds to of our a known knowledge dilute of case MLPH and amutations, known carrier, leadinga premature to dilute stop-gain phenotypes point mutationin domestic was species. identified within MLPH. This work adds to our knowledge of MLPH mutations, leading to dilute phenotypes in domestic species. 2. Materials and Methods 2. Materials and Methods 2.1. Sample Collection 2.1. Sample Collection All sheep were sampled in accordance with the Cornell University Institutional Animal Care & Use CommitteeAll sheep were(Protocol sampled #2014-0121). in accordance Owner with consen thet Cornellwas given University prior to Institutional sample collection Animal for Care & privatelyUse Committee owned (Protocolsheep. Whole #2014-0121). blood was Owner collected consent from was the given jugular prior vein to sample via 10-mL collection vacutainers for privately containingowned sheep. K2EDTA, Whole and blood genomic was collectedDNA was from extracted the jugular following vein the via Qiagen 10-mL Puregene vacutainers Protocol containing (GentraK2EDTA, Systems, and genomic Inc. Minneapolis, DNA was MN, extracted USA). following The genomic theQiagen DNA was Puregene stored at Protocol −80 ℃ (Gentrauntil it was Systems, sequenced.Inc. Minneapolis, MN, USA). The genomic DNA was stored at 80 C until it was sequenced. − ◦ TheThe dilute dilute phenotype phenotype was was visually visually characterized characterized by by diluted diluted pigment pigment in inthe the nonwhite nonwhite portions portions of ofthe the fleece. fleece. An An example example of of dilutedilute andand non-dilutenon-dilute JacobsJacobs can be be seen seen in in Figure Figure 1.1 .The The two two Jacobs Jacobs used used for forwhole-genome whole-genome sequencing sequencing were were unrelated unrelated within within five five generations. generations. Additional Additional dilute dilute Jacobs Jacobs were were sourced sourcedfrom an from unrelated an unrelated flock. flock. In total, In total, 22 dilute 22 dilute Jacobs, Jacobs, 13 13 known known carriers, carriers, and and 26 26 non-dilute non-dilute JacobsJacobs were wereavailable available for testing. for testing. The carriersThe carriers were were determined determined via pedigreevia pedigree analysis, analysis, using using the Jacobthe Jacob Sheep Sheep Breeders Breeders Association pedigree database [17]. An additional 163 sheep that were not dilute, Association pedigree database [17]. An additional 163 sheep that were not dilute, representing the Icelandic, representing the Icelandic, Karakul, California Red, Romeldale, Romney, Finnsheep, Lincoln, and Karakul, California Red, Romeldale, Romney, Finnsheep, Lincoln, and Shetland breeds, were used for Shetland breeds, were used for validation testing. validation testing. (a) (b) Figure 1. Cont. Genes 2020, 11, 618 3 of 8 Genes 2020, 11, x FOR PEER REVIEW 3 of 8 (c) (d) FigureFigure 1.1. PhotosPhotos ofof dilute dilute (lilac) (lilac) and and non-dilute non-dilute Jacob Jacob sheep sheep that werethat were used forused whole-genome for whole-genome sequencing aresequencing in panels are (a) andin panels (b): (a ()a and) and (c )(b are): ( examplesa) and (c) ofare the examples lilac dilution of the in lilac Jacob dilution sheep; (inb) Jacob and ( dsheep;) are examples (b) ofand non-dilute (d) are examples Jacob sheep. of non-dilute Jacob sheep. 2.2. Whole Genome Sequencing 2.2. Whole Genome Sequencing TruSeq PCR-Free libraries were prepared for a known dilute case, a known dilute carrier, TruSeq PCR-Free libraries were prepared for a known dilute case, a known dilute carrier, and andsixteen sixteen additional additional non-dilute non-dilute control control samples samples from other from breeds. other The breeds. libraries The were libraries sequenced were sequenced using using150 bp 150 paired-end bp paired-end reads readson an on Illumina an Illumina HiSeq HiSeq X Ten X Tenplatform platform to generate to generate approximately approximately 20x 20x coveragecoverage perper individual.individual. TheseThese sequencessequences havehave beenbeen deposited deposited in in NCBI’s NCBI’s sequence sequence read read archive archive (SRA) and(SRA) can and be foundcan be underfound theunder
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