Linkage map Genetic and physical assignment of equine microsatellites began almost ten years ago.
BREEN et al. (1997) isolated 20 equine microsatellites from a genomic phage library and mapped them by linkage mapping and FISH.
GODARD et al. (1997) assigned 36 new horse microsatellites, 11 of them from plasmid libraries and 25 from a cosmid library.
The first equine linkage map included 140 markers (LINDGREN et al., 1998) and a more extensive linkage map consisted of 161 loci in 29 linkage groups for 26 autosomes (GUERIN et al., 1999).
The first map covering all autosomes and the sexchromosomes using 353 microsatellite-markers was generated by SWINBURNE et al. (2000).
The microsatellites were mapped to 42 linkage groups and covered 1780 cM of the horse genome.
A second generation linkage map was published by the International Equine Gene Mapping Workshop (GUERIN et al. 2003).
This linkage map was based on testing 11 Arch.
Tierz. 50 (2007) 1 503 half-sibling offspring from 13 sire families.
The map included 344 markers in 34 linkage groups representing all 31 autosomes, but neither the X- nor the Ychromosome.
The linkage groups covered 2262 cM with an average interval between loci of 10.1 cM, ranging from 0 to 38.4.
Another 61 new horse microsatellite loci were assigned by SWINBURNE et al. (2003).
TOZAKI et al. (2004) reported the characterization of 341 newly isolated microsatellite markers of which 256 were assigned to equine chromosomes.
PENEDO et al. (2005) added 359 microsatellites to the second generation linkage map.
Alltogether, this linkage map consisted of 766 markers assigned to the 30 autosomes and the X-chromosome spanning 3740 cM with an average marker density of 6.3 cM.
SWINBURNE et al. (2006) generated a linkage map including 742 markers in 32 linkage groups according to the 31 autosomes and the X-chromosome.
All linkage groups together span 2772 cM with an average interval of 3.7 cM between the markers.
Chromosomal abnormalities There exist several chromosomal abnormalities in the horse.
Of great interest and therefore well analyzed are those concerning the sex-chromosomes and influencing the fertility of mares: The most common abnormality in mares, X0 Gonadal Dysgenesis (X monosomy), is characterised by the lack of one X-chromosome (63,X0) and was primarily described by HUGHES et al. (1975).
This defect was accompanied with infertility of the affected mare.
POWER (1986) reported another abnormality in horses, the XY Gonadal Dysgenesis.
The affected horses` phenotype is female, but their genotype is 64,XY leading to infertility (BOWLING et al., 1987).
There exist also infertile mares with the genotype 65,” (CHANDLEY et al., 1975).
KAKOI et al. (2005) published a statistical evaluation of sex chromosome abnormalities and analyzed data of 17471 light-breed foals with the result that 0.15 % of the analyzed population showed an XO-, 0.02% an XXY- (and/ or mosaics/chimaeras) and 0.01% an “-genotype.
Unlike the sex chromosomes, chromosomal abnormalities of the autosomes are rarely encountered.
Cases of trisomy are similar to human Downs and associated with mental retardation failure to thrive (LEAR et al., 1999).
Coat colours There exist several genetically characterized major genes that influence the coat colour of a horse: Agouti-gene, Extension-gene, Cream dilution gene, Tobiano-gene, Whitegene, Greying hair-gene, Dun-gene, Roan-gene, Sabino-gene, Silver-gene, and the Leopard Complex-gene.
Knowledge about the inheritance of coat colours is very important for the breeders, so it is comparatively well explorated and for several genes exist gene tests, too.
Chromosomal locations and mutations of genes associated with equine coat colours are summarized in Table.
The White-gene and the Greying hair-gene can mask all the other coat colour genes, so they are mentioned first.
White-gene (W-gene) and Sabino spotting Horses with the dominant allele “W” lack pigment in skin and hair, so their coat colour is white at birth, but eyes are dark or sometimes blue.
The W-mutation was mapped to 12 STÜBS; DISTL: Horse genome a region of ECA3q22 where the equine KIT gene is located (MAU et al., 2004).
The homozygous “WW” is lethal at a very early stage of pregnancy as it is in mice, too.
Since the action of the dominant white allele seems not always to be fully penetrant, some horses homozygously “WW” are born alive with the phenotype of sabino spotting.
All non-white horses are homozygous recessive “ww”.
In contrast to the greying gene, horses with the dominant “W” are not able to produce any pigment, white horses with the “G”-gene instead can produce pigment but lose their pigment with aging.
Sabino pattern is characterized by irregulary bordered white patches on the lower limbs and face and often includes belly and interspersed white hairs on the midsection.
Sabino spotting is found in many light horse breeds such as Tennessee walking horse, Missouri Foxtrotter, Shetland pony and American Paint Horse.
A single nucleotide exchange in the 3’-splice site of intron 16 of the equine KIT gene causes a partial skipping of exon 17 and the Sabino spotting (BROOKS and BAILEY, 2005).
Furthermore, close association between KIT polymorphisms and roan coat colour was detected in horses (MARKLUND et al., 1999).
Greying-gene (G-gene) The dominant allele “G” is responsible for progressive greying in hairs.
If a foal that possesses the allele “G” is born coloured it will progressively turn white as an aged animal.
The Grey-locus was mapped to ECA25 by SWINBURNE et al. (2002) and by HENNER et al. (2002).
The mapping of the G-gene was of particular importance because the Grey-gene and the appearance of melanomas in horses are associated: grey horses get melanomas with a frequency of at least 80% in horses older than 10 years whereas melanomas are rare in non-grey horses.
SWINBURNE et al. (2002) localized the G-locus 13 cM proximal of the marker TKY316 and 17 cM distal of the marker UCDEQ464 using a whole genome scan.
PIELBERG et al. (2005) refined the grey-locus to a region smaller than 6.9 Mb on ECA25 using comparative mapping to mouse and human.
In this refined region, no obvious candidate genes for pigmentation disorders could be identified.
Several possible candidate genes responsible for different coat colours including agoutisignaling-protein (ASIP), melanocortin-1-receptor (MC1R), tyrosinase-related protein 1 (TYRP1) and silver homolog (SILV, PMEL17) had been excluded before (RIEDER et al., 2001; LOCKE et al., 2002).
Agouti-gene (A-gene) The Agouti locus with the dominant “A” and recessive “a” allele is responsible for the distribution pattern of black hair.
The interaction with the extension-gene is responsible if the horse is bay or black: A horse that is homozygous recessive “aa” will be black if it also possesses a dominant “E” allele.
If a horse possesses at least one “A” allele together with the “E” allele, it will be bay.
However, if a horse is homozygous recessive “ee”, it will look sorrel or chestnut, irrespective if it carries an “A” or “a”.
This is important for the breeders, because it is possible that a sorrel or chestnut horse can also produce blacks.
RIEDER et al. (2001) characterized equine MC1R (melanocortin-1-receptor) and ASIP (agouti signaling protein), and completed a partial sequence of TYRP1.
They detected an 11-bp deletion in exon 2 (ADEx2) of ASIP which was completely associated with horse recessive black coat color in horses of 9 13 Arch.
Tierz. 50 (2007) 1 different breeds.
The frameshift initiated by ADEx2 was supposed to act as a loss-offunction ASIP mutation.
Extension gene (E-gene) The Extension locus controls the expression of black pigment in horses.
The equine melanocyte stimulating hormone receptor (MC1R) on ECA3 encodes the Extension locus (MARKLUND et al., 1996).
A missense mutation in MC1R was associated with light colour, whereas the wildtype allele corresponded to dark pigmentation.
A black or bay horse possesses at least one “E” allele.
A horse that is homozygous “ee” is either chestnut or sorrel.
For horse breeders where black colour is valued, it is important, if a horse is homozygous “EE”, because that means that it will never have a chestnut or sorrel foal.
Cream dilution gene (C-gene) The dominant “C” allele causes a reduction in red pigment in hairs.
A sorrel horse inheriting one “C” allele is palomino (ee/Cc), a sorrel inheriting “C/C” is cremello (ee/CC).
A bay horse inheriting one “C” allele is buckskin (E-/Cc) and a horse homozygous for “C” is a perlino (E-/CC).
It is also possible that grey or dun horses carry the “C” allel.
The C-locus was localized to ECA21 and TYR (tyrosinase) could be excluded as candidate for the cream dilution gene (LOCKE et al., 2001).
MARIAT et al. (2003) identified the causal mutation similarly to mice and humans in exon 2 of the membrane associated transporter protein (MATP) gene mapping to ECA21p17.
A gene test based on this G to A transition could be developed to control if a horse carries a dominant “C” allele.
Tobiano-gene (To-gene) The “To” allele is dominantly inherited and is responsible for white spotting characterized by distinct borders crossing the dorsal midline and including at least one if not all four limbs.
There was identified a MSPI polymorphism for the Tobiano-locus in intron 13 of the equine homologue of the proto-oncogene c-kit (KIT) gene (KM1 locus) which is strongly associated with the Tobiano gene but not causative (BROOKS et al., 2002).
If a horse does not possess the Tobiano-allele, the test result will be designated KM0/KM0.
If a horse carries one “To” allele, it will be tested KM0/KM1, and if the test is KM1/KM1, the horse is probably a homozygous Tobiano.
However, solid-coloured horses can also possess the KM1 allele.
This test is useful for breeders valuing homozygous Tobianos, because they will always produce spotted foals.
Silver-gene (Z-gene) A mutation in the Silver (PMEL17) gene had recently been identified that produces in black horses a chocolate coat colour with flaxen mane and tail and in bay horses lightened coat colour in lower legs and flaxen mane and tail (BRUNBERG et al., 2006).
This mutation has no effect on chestnut-coloured horses.
A missense mutation in exon 11 changing arginine to cysteine (Arg618Cys) was likely to be causative as complete association with the Silver phenotype was observed across several horse breeds.
A further silent mutation in intron 9 was also completely associated with the Silver phenotype. 14 STÜBS; DISTL: Horse genome Appaloosa coat colour TERRY et al. (2004) investigated the appaloosa coat colour which is characterized by several different spotting patterns ranging from a few white specks on the rump to an almost completely white animal (Table).
They excluded the KIT gene as possible candidate gene causing Rw colour pattern in mice and also the candidate genes microphthalmia-associated transcription factor (MITF) and mast cell growth factor (MGF) (TERRY et al., 2001, 2002).
They found that the autosomal incompletely dominant gene LP (leopard complex) responsible for the appaloosa coat pattern in horses mapped to ECA1q (TERRY et al., 2004). Table Molecular genetic characterization of coat colour loci in horse (Molekulargenetische Charakterisierung von Farbgenorten beim Pferd) Locus Gene ECA Mutation Reference Agouti ASIP 22q15-q16 11 bp deletion RIEDER et al. (2001) Extension MC1R 3p12 C>T missense MARKLUND et al. (1996) mutation Cream MATP 21p17 G>A missense MARIAT et al. (2003) mutation Sabino KIT 3q22 T>A mutation BROOKS and BAILEY (2005) (splice mutation) Tobiano KIT 3q22 C>G missense BROOKS et al. (2002) mutation Silver PMEL17 6q23 C>T missense BRUNBERG et al. (2006) mutation ECA: Equus caballus autosome. Equine genetic diseases and the development of gene tests The most important information breeders take from gene investigation are probably new results as to diseases or phenotypic features.
While inheritance of colours is usually comparatively simple with different alleles that are either dominant or recessive responsible for all colours, investigation of inheritance of diseases is often much more complicated, for example multifactorial and influenced by lots of different genes.
There are 188 diseases reported in the horse that are discussed to be inherited.
For 20 well-explorated diseases only a single locus is responsible for the appearance.
This is probably one of the reasons for the fact that there are only a few gene tests available for important diseases but for many of the possibly inherited diseases in the horse the inheritance is still unknown.
Monogenic equine diseases Lethal White Foal Syndrome (LWFS) The Lethal White Foal Syndrome is observed in horse breeds with white coat spotting patterns called overo, eg, in Paints and Pintos.
Affected foals are almost completely white and die shortly after birth due to severe intestinal blockage resulting from a lack of nerve cells in the distal portion of the large intestine (aganglionic megacolon).
The disease is similar to Hirschsprung disease in humans.
As the Hirschsprung disease is caused by a mutation in the endothelian B receptor gene (EDNRB), METALLINOS et al. (1998) investigated the influence of the EDNRB in horses with Lethal White Foal Syndrome and found an association between a missense mutation in the EDNRB-gene 15 Arch.
Tierz. 50 (2007) 1 and the appearance of LWFS like in humans for the Hirschsprung disease.
YANG et al. (1998) could show that a dinucleotide TC>AG mutation was associated with LWFS when homozygous and with the overo phenotype when heterozygous.
Herlitz junctional epidermolysis bullosa (epitheliogenesis imperfecta) The pathological signs of epitheliogenesis imperfecta closely match a similar disease in humans known as Herlitz junctional epidermolysis bullosa, which is caused by a mutation in one of the genes (LAMA3, LAMB3 and LAMC2) coding for the subunits of the laminin 5 protein.
Herlitz junctional epidermolysis bullosa (HJEB) is a lethal disease that causes blistering of the skin and mouth epithelia, and sloughing of hooves in newborn foals, especially in American Saddlebred horses and Belgian draft horses (JOHNSON et al., 1998).
Pedigree studies demonstrated that the trait followed a monogenic autosomal recessive inheritance pattern and a genetic mapping study revealed that HJEB in American Saddlebred horses was linked to microsatellites on ECA8q where LAMA3 is also located (LIETO and COTHRAN, 2003).
SPIRITO et al. (2002) detected a cytosine insertion in exon 10 in the LAMC2 gene as being responsible for HJEB in Belgian draft horses and BAIRD et al. (2003) developed a gene test that works with hair of the horses and is now available for owners of registered horses.
The same mutation was found to be associated with the same condition in the French draft horse breeds, Trait Breton and Trait Comtois (MILENKOVIC et al., 2003). Hyperkalemic periodic paralysis Hyperkalemic periodic paralysis (HYPP) is an inherited disease of the muscles that causes attacks of paralysis that can lead to sudden death that especially affects American Quarter horses.
It is inherited as an autosomal codominant genetic defect so that heterozygous horses are affected, too (ZEILMANN, 1993).
HYPP is the result of a missense mutation of the gene encoding the α-chain of the adult muscle sodium channel.
RUDOLPH et al. (1992) described the point mutation in transmembrane domain IVS3 that is responsible for the occurrence of the disease.
Even though the attacks can be treated with azetazolamide (KOLLIAS-BAKER, 1999) and the disease will not always lead to death, it is useful to test horses if they are carriers or not. Severe Combined Immunodeficiency (SCID) SCID is an inherited disease known in different species that always causes an early death of affected animals because of the incapability to generate antigene-specific immune responses; there exists a comparative study between the different mechanisms that lead to SCID in humans, mice, horses and dogs (PERRYMAN, 2004).
SCID is recessively inherited in Arabian horses.
Horses affected with SCID cannot react in a natural way of protection against diseases.
They do not develop the necessary active protection reactions because they lack intact lymphocytes.
Due to this reason, affected foals will not become older than six months.
SHIN et al. (1997) tested candidate genes from the mouse and could show that SCID is caused by a frameshift mutation in the gene for DNA-dependent protein kinase catalytic subunit (DNA-PK) mapping to horse chromosome 9.
This mutation results in the lack of a full-length kinase.
Glycogen Branching Enzyme Deficiency (GBED) GBED is a glycogene storage disease similar to the human glycogen storage disease type IV.
The disease is lethal for the affected foals with a great variability of 16 STÜBS; DISTL: Horse genome symptoms ranging from abort or stillbirth until being euthanized due to weakness.
VALBERG et al. (2001) described the disease in American Quarter horses.common to GBED are the accumulation of unbranched polysaccharides in tissues and a profound decrease of glycogen branching enzyme activity in cardiac and skeletal muscle as well as in liver and peripheral blood cells of affected foals.
The pedigree analysis supported an autosomal recessive mode of inheritance.
WARD et al. (2003) mapped the GBE1 gene to ECA26q12-q13, and later on, detected the C- to A-mutation at base 102 of the GBE1 gene causing the disease (WARD et al., 2004).
An autosomal recessive mode of inheritance was confirmed.
It is now possible to test horses whether they are carriers of the GBE1 allele.
Genetically complex equine diseases Osteochondrosis (OC) Osteochondrosis (OC) is a developmental orthopaedic disorder frequently observed in young horses (VAN DE LEST et al., 1999).
Signs of osteochondrosis are lesions of the cartilage in the joints like subchondral fractures, subchondral cysts, wear lines, chondromalacia, cartilage flaps and joint mice or free joint bodies (chips).
Hereditary factors play an important part in the pathogenesis of OC.
An optimized microsatellite marker set for complete genome scans in horses was developed including 155 highly polymorphic markers equally distributed at a distance of about 20 cM.
Data from 14 half-sib families of Hanoverian Warmblood horses were analysed using this marker set to detect quantitative trait loci (QTL) with significant influence on the development of OC (BÖNEKER et al., 2006; DIERKS et al., 2006).
QTL for osteochondrosis in fetlock and hock joints were found on horse chromosomes 2, 3, 4, 5, 15, 16, 19, and 21.
In a population of South German coldblood horses a further whole genome scan for OC in fetlock and hock joints was carried out (WITTWER et al., 2006; WITTWER and DISTL, 2006).
In total, 17 chromosome-wide significant QTL were found on different equine chromosomes with influence on the development of OC in fetlock and hock joints.
Navicular disease Navicular disease (navicular syndrome or podotrochlosis) is a chronic and usually progressive, degenerative alteration of the equine podotrochlea (RIJKENHUIZEN, 1989).
Pathological alterations can primarily affect the navicular bone (os sesamoideum distale), the navicular bursa (bursa podotrochlearis) or the distal end of the deep digital flexor tendon.
The disease may be part of the osteoarthritis complex (SVALASTOGA and SMITH, 1983).
A microsatellite marker set to be applied in Hanoverian warmblood horses for a whole genome scan was prepared and then a whole genome scan in 144 descendants of 17 Hanoverian warmblood stallions was performed.
The genotyped horses were randomly sampled from the whole Hanoverian warmblood breeding district.
QTL on different horse chromosomes were identified such as on ECA2, 3, 4, and 10 (DIESTERBECK et al., 2006).
According to SVALASTOGA and SMITH (1983) increased bone marrow pressure and lengthened contrast passage indicate similarities between osteoarthritis (OA) in humans and navicular disease in horses.
About 50 different positional candidate genes have been reported for OA in humans.
These candidate genes encode different types of collagens, hormone receptors and interleukin receptors, growth factors and metalloproteinases. 17 — An update of chromosomal abnormalities in mares.
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OTTMAR DISTL* Institute for Animal Breeding and Genetics University of Veterinary Medicine Hannover Bünteweg 17p 30559 HANNOVER GERMANY *Corresponding Author E-Mail: firstname.lastname@example.org
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