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Mar Biotechnol (2012) 14:237–244 DOI 10.1007/s10126-011-9407-2

ORIGINAL ARTICLE

A Microsatellite Linkage Map of Striped Bass (Morone saxatilis) Reveals Conserved Synteny with the Three-Spined Stickleback (Gasterosteus aculeatus) Sixin Liu & Caird E. Rexroad III & Charlene R. Couch & Jan F. Cordes & Kimberly S. Reece & Craig V. Sullivan

Received: 27 May 2011 / Accepted: 2 September 2011 / Published online: 4 October 2011 # Springer Science+Business Media, LLC (outside the USA) 2011

Abstract The striped bass (Morone saxatilis) and its relatives (genus Morone) are of great importance to fisheries and aquaculture in North America. As part of a collaborative effort to employ molecular genetics technologies in striped bass breeding programs, we previously developed nearly 500 microsatellite markers. The objectives of this study were to construct a microsatellite linkage map of striped bass and to examine conserved synteny between striped bass and three-spined stickleback (Gasterosteus aculeatus). Of 480 microsatellite markers screened for polymorphism, 289 informative markers were identified and used to genotype two half-sib mapping families. Twenty-six linkage groups were assembled, and only two markers remain unlinked. The sex-averaged map spans 1,623.8 cM with an average marker density of 5.78 cM per marker. Among 287 striped bass microElectronic supplementary material The online version of this article (doi:10.1007/s10126-011-9407-2) contains supplementary material, which is available to authorized users. S. Liu (*) : C. E. Rexroad III USDA/ARS National Center of Cool and Cold Water Aquaculture, Kearneysville, WV 25430, USA e-mail: [email protected] C. R. Couch Department of Genetics, North Carolina State University, Raleigh, NC 27695, USA J. F. Cordes : K. S. Reece Department of Environmental and Aquatic Animal Health, Virginia Institute of Marine Science, Gloucester Point, VA 23062, USA C. V. Sullivan Department of Biology, North Carolina State University, Raleigh, NC 27695, USA

satellite markers assigned to linkage groups, 169 (58.9%) showed homology to sequences on stickleback chromosomes or scaffolds. Comparison between the stickleback genome and the striped bass linkage map revealed conserved synteny between these two species. This is the first linkage map for any of the Morone species. This map will be useful for molecular mapping and marker-assisted selection of genes of interest in striped bass breeding programs. The conserved synteny between striped bass and stickleback will facilitate fine mapping of genome regions of interest and will serve as a new resource for comparative mapping with other Perciform fishes such as European sea bass (Dicentrarchus labrax), gilthead sea bream (Sparus aurata), and tilapia (Oreochromis ssp.). Keywords Striped bass . Microsatellite . Linkage map . Synteny . Three-spined stickleback

Introduction Striped bass (Morone saxatilis) are native to coastal estuaries and rivers along the east coast of North America and the Gulf of Mexico. This species is economically important in the United States due to its value as an aquaculture species and in supporting commercial and recreational fisheries. Due to habitat degradation and overexploitation, the striped bass fishery experienced significant population declines in the mid-1970s. The hybrid between striped bass and white bass (Morone chrysops) exhibits improved performance in captivity with regard to growth, survival, hardiness and disease resistance. Therefore, hybrid striped bass farming grew rapidly from 1987 to 2000 but has remained relatively static in recent years due to high production costs (Garber and Sullivan 2006). Selective

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breeding for traits associated with aquaculture production efficiency is one of the keys to reduce production costs and to promote continued aquaculture industry expansion (Garber and Sullivan 2006). Molecular markers play an important role in modern plant and animal breeding (Liu and Cordes 2004; Dekkers 2004). Microsatellite markers are highly polymorphic, abundant, and easy to use and are the marker of choice for many livestock species. They have been used for construction of genetic maps, characterization of broodstocks, mapping traits of interest, identification of individuals, and parentage assignment in aquaculture species (Chistiakov et al. 2006). As part of a collaborative effort to employ molecular genetics technologies in striped bass breeding programs, nearly 500 microsatellite markers were developed from repeat-enriched libraries (Rexroad et al. 2006; Couch et al. 2006). However, a genetic linkage map for striped bass has not previously been reported. Comparative mapping has led to the identification of conserved synteny among fish species (Sarropoulou et al. 2008; Sarropoulou and Fernandes 2010; Rexroad et al. 2005). Whole-genome reference sequences are available for five model fish species, zebrafish (Danio rerio), medaka (Oryzias latipes), three-spined stickleback (Gasterosteus aculeatus), fugu (Fugu rubripes), and puffer fish (Tetraodon nigroviridis). These genome sequences have facilitated extensive comparisons between the model species and non-model species lacking a sequenced genome. Stemshorn et al. (2005) reported that 45% of microsatellite markers mapped in European sculpin (Cottus gobio) showed significant homology with the Tetraodon nigroviridis genome sequence. However, among 525 microsatellite markers and 21 genebased markers mapped in tilapia (Oreochromis spp.), only 61 markers showed significant homology with the genome sequence of Tetraodon nigroviridi (Lee et al. 2005). Kucuktas et al. (2009) identified regions of conserved synteny between catfish and model species. Conserved syntenies between the linkage groups of rainbow trout (Oncorhynchus mykiss) and model fish species were also identified by comparative mapping (Rexroad et al. 2008; Guyomard et al. 2006). Xia et al. (2010) reported substantial macro-synteny and extensive marker co-linearity between grass carp (Ctenopharyngodon idella) and zebrafish. Extensive genomic resources, such as linkage maps (Chistiakov et al. 2005, 2008; Franch et al. 2006), radiation hybrid maps (Guyon et al. 2010; Sarropoulou et al. 2007), and BAC-end sequences (Kuhl et al. 2010), have been developed for European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata), two important aquaculture species belonging to the order Perciformes. Sequence comparisons revealed conserved synteny between model species and these two aquaculture species. The highest number of significant matches was obtained against

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stickleback (Chistiakov et al. 2008; Guyon et al. 2010; Kuhl et al. 2010), a species belonging to the order Gasterosteiformes. This is consistent with the closer phylogenetic relationship between Perciformes and Gasterosteiformes (Sarropoulou et al. 2008). Since striped bass also belongs to the order Perciformes, the sequences of striped bass microsatellite markers mapped in this study were compared with the genome sequence of stickleback to examine the syntenic relationships between these two species. The conserved synteny between striped bass and stickleback will facilitate fine mapping of genome regions of interest and will serve as a new resource for comparative mapping with other Perciform fishes such as European sea bass, gilthead sea bream, and tilapia.

Materials and Methods Mapping Populations Two half-sib families that shared a common dam were used to construct the striped bass genetic map. The dam was a captive wild-caught female from the Roanoke River. The sires were produced by crossing captive-born F1 female offspring of wild parents from the Santee-Cooper reservoir system with males from a line of F2 fish from Chesapeake Bay that had been domesticated for several generations (Woods 2001). The two half-sib families were chosen for linkage mapping because preliminary genotyping of the fish at six microsatellite loci revealed them to be the most variable of six half-sib families from the same dam, with large numbers of informative meioses for detection of linkage disequilibrium (C.R. Couch and C.V. Sullivan, unpublished data). Additionally, preliminary evaluation of data on quantitative traits such as length and weight, body shape, weight of viscera and gonads, and fillet yield of 18-month-old, market-sized fish indicated a high degree of variation within and between these two half-sib families, which would facilitate discovery of quantitative trait loci once the genetic linkage map was developed. Fin clips were collected from the three parents and 93 or 94 offspring from each of the two mapping families. DNA was extracted using a phenol-chloroform method as described in Sambrook and Russell (2001). Microsatellite Genotyping We screened a total of 480 markers in the present study, including 147 from Couch et al. (2006), 328 from Rexroad et al. (2006), and five from miscellaneous sources (Brown et al. 2003; Garcia de Leon et al. 1995; Roy et al. 2000). Initially, markers were screened using a panel comprised of the three parents and six progeny from each family.

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Informative markers were then used to amplify the full panel of progeny from the two families. In order to minimize the number of PCR reactions that would have to be performed, amplifications were done as multiplexed reactions containing primers for up to four markers, each labeled with one of four different fluorescent markers (Additional file 1 of the “Electronic supplementary material”). Markers in the same multiplexed groups have similar annealing temperatures and minimal allele size overlap among the four markers. In order to maximize the number of markers that could be incorporated into the genetic linkage map, markers that would not amplify as part of a multiplexed reaction were amplified individually. Multiplex PCR amplifications were carried out using the Type-it Kit from Qiagen (Valencia, CA, USA). The total reaction volume was 5 μl, containing 0.5 μl DNA (~10 ng/ μl) template, 1×Type-it multiplex PCR master mix, 0.3 μM forward primer and 1.5 μM reverse primer (final concentration of the four primers together), and 30 nM each of fluorescent primer tags (Applied Biosystems). For markers that were not incorporated into multiplex reactions and/or that would not amplify using this kit, PCR amplifications were carried out in 5-μl reactions containing 0.5 μl DNA (~10 ng/μl), 1.5 mM MgCl2, 0.2 mM dNTP mix (Invitrogen), 1× PCR buffer (Invitrogen), 0.25 μM forward primer (Operon), 1.0 μM reverse primer, 0.3 μM color primer (Applied Biosystems), and 0.125 U Taq DNA polymerase (Invitrogen). Thermal cycling parameters consisted of initial denaturation at 95°C for 3 min, 35 cycles each of 94°C for 30 s, marker-specific annealing temperature (Additional file 1 of the “Electronic supplementary material”) for 90 s, and 72°C for 30 s, followed by a final extension at 72°C for 30 min. One microliter of each amplification product was denatured by addition of 9.0 μl formamide, heated to 95°C for 5 min, and genotyped on an ABI 3130 DNA analyzer. The GeneScan™ 500 LIZ (Applied Biosystems) internal size standard was added to each sample for accurate and consistent scoring of alleles. Alleles were scored using GeneMarker® software v. 1.75 (SoftGenetics LLC, State Park, PA, USA). Linkage Analysis Genotype data were formatted using MAKEPED for the LINKAGE (Lathrop et al. 1984) program and checked for inconsistencies with Mendelian inheritance using PEDCHECK (O’Connell and Weeks 1998). The data were transformed into CRIMAP (Lander and Green 1987) format using in-house scripts. MULTIMAP (Matise et al. 1994) was used to construct the genetic maps. Markers were assigned into linkage groups with the parameters of LOD≥ 3 and recombination fraction r≤0.3. The framework map

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for each linkage group was constructed with default parameters, and markers were added to the comprehensive map by lowering the LOD threshold one integer at a time and starting with the previous order. This comprehensive map is a sex-averaged genetic map. Sex-specific maps were constructed based on the marker order of the comprehensive map. Software MapChart (Voorrips 2002) was used to draw the linkage maps. Sequence Similarity Searches The clone sequences of markers mapped onto the linkage map in this study were downloaded from GenBank of the NCBI (National Center for Biotechnology Information) and were masked with the RepeatMasker web server (http:// repeatmasker.org). The masked sequences were used as queries to search the masked genomic sequences of threespined stickleback (Assembly: BROAD S1, Feb 2006; http://www.ensembl.org) using the default parameters for BLASTn. Hits were considered significant only if the e-value of the best hit was equal or lower than 10−5 and the e-value of second best hit was at least 104-fold larger than that of the best hit.

Results Among the 480 previously reported microsatellite markers (Couch et al. 2006; Rexroad et al. 2006), 31 markers were eliminated from further analysis due to poor amplification or difficulty in scoring the products. For the remaining 449 markers, 289 markers (64.4%) were informative for at least one of the two mapping families. The number of informative meioses ranged from 74 to 374 with an average of 261 (Additional file 2 of the “Electronic supplementary material”). Among the 289 informative markers, only two markers, MSM1261 and MSM1565, were not linked with other markers in the data set at a threshold of LOD≥3 and recombination fraction of r≤ 0.3. The remaining 287 markers were assembled into 26 linkage groups (Fig. 1). The number of markers per linkage group ranges from 2 to 24 (Table 1). A total of 192 markers were ordered onto the framework maps with a threshold of LOD≥3. The remaining markers were placed onto the comprehensive maps by retaining the order of the framework map and lowering the LOD threshold. The sex-averaged genetic map (Fig. 1) spans 1,623.8 cM with an average marker density of 5.78 cM per marker. The female genetic map (Additional file 3 of the “Electronic supplementary material”) spans 1,581.0 cM, and the male genetic map (Additional file 4 of the “Electronic supplementary material”) spans 1,834.1 cM. Therefore, the overall female/male recombination ratio is

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Fig. 1 Sex-averaged linkage map of striped bass. The map distances are in Kosambi cM. The linkage groups (LG) are ordered according to the number of microsatellite markers in each group. All markers were assigned to each linkage group with LOD≥3. The markers on the

framework map are in bold but not italic font (LOD≥3); the rest of the markers were placed onto the comprehensive map with lower confidence about their positions—underline font LOD≥2, italic but not bold font LOD≥1, and bold italic font LOD≥0

0.86:1. However, this ratio varies by linkage group, ranging from 0.42:1 to 1.52:1 (Table 1). Among the 169 markers (58.9%) that showed significant homology to sequences of the stickleback genome, 152 markers were assigned to stickleback chromosomes and 17 markers were assigned to scaffolds with unknown chromosomal locations (Table 2). A comparison between the stickleback genome and the striped bass linkage map revealed the conserved synteny between these two species (Table 2; Fig. 2). Stickleback chromosomes 1, 4, and 7 showed homology with two striped bass linkage groups. Only one striped bass marker showed homology with stickleback chromosome 6. Other stickleback chromosomes had one-to-one relationships with the striped bass linkage groups. Even though highly conserved synteny between striped bass and stickleback was observed at the

chromosomal level, closer examination of marker orders revealed a complex co-linearity within each linkage group (Fig. 2; Additional file 5 of the “Electronic supplementary material”).

Discussion Linkage Map Among the 289 informative microsatellite markers, only two markers are not linked to any other markers, indicating that the current linkage map provides a reasonably good coverage of the striped bass genome. The sex-averaged genetic map spans 1,623.8 cM, which is similar to the map lengths of European sea bass (Chistiakov et al. 2005),

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Table 1 Distribution of markers and length of each linkage group of striped bass LG

Number of loci

Length (Kosambi cM) Sex-averaged

F:M

Female

Male

1

24a

114.2

128.9

84.9

1.52

2 3

17 16

4 5 6

16a 15 14

62.3 122.7 70.8

73.7 121 73.8

52.1 181 61.8

1.41 0.67 1.19

7 8 9

14b 14 14

93.6 49.2 76.2

86.9 57.6 70.1

201.6 38.5 84.3

0.43 1.50 0.83

57.9 64.7

66.4 66.7

54.0 62.6

1.23 1.07

10

13

85.3

97.4

84.1

1.16

11 12

12 12

78.9 65

69 53.5

96.3 61.7

0.72 0.87

13

12

99.6

78.4

110.4

0.71

14 15 16

12 11 11

17 18

10a 9

77.3 73 63.7 42.3 51.3

69.3 65.7 49.5 36.6 55.4

103.1 91.4 67.8 50.8 68.9

0.67 0.72 0.73 0.72 0.80

19 20 21

9 8 8

63.4 56.3 72.1

70.6 51.1 69.7

60.5 46.9 73.5

1.17 1.09 0.95

22 23

4 4

46.5 30.7

38.8 25.9

55.1 34.4

0.70 0.75

24 25 26

3 3 2

5.2 1.6 0

3.1 1.9 0

7.3 1.1 0

0.42 1.73

Total

287

1,623.8

1,581.0

1,834.1

0.86

a

One marker could not be ordered uniquely onto the genetic map

b

Three markers could not be ordered uniquely onto the genetic map

marker-assisted selection, map-based cloning, and comparative mapping. This is the first linkage map for striped bass and will facilitate the discovery, genetic mapping, and cloning of genes that affect biochemical processes underlying important phenotypic traits. Sex-Specific Recombination Differences in recombination rates between sexes have been well documented. In extreme cases, it was discovered that there is no recombination in male Drosophila and there is no recombination in female Bombyx bumblebees (Haldane 1922), while in both cases recombination does occur in the opposite sex. Less frequent recombination in the heterogametic (male) sex was observed in mammals such as humans (Kong et al. 2002), mice (Shifman et al. 2006), and dogs (Mellersh et al. 1997); however, there are some exceptions. For example, the female-to-male recombination ratio is 0.79 in domestic sheep (Crawford et al. 1995), and severely reduced recombination in females was reported and validated in gray, short-tailed opossum, Monodelphis domestica (Samollow et al. 2004, 2007). Higher recombination rates in females also were reported in several fish species such as medaka (Naruse et al. 2000), rainbow trout (Sakamoto et al. 2000; Rexroad et al. 2008), brown trout (Gharbi et al. 2006), Atlantic salmon (Moen et al. 2004), zebrafish (Singer et al. 2002), and catfish (Waldbieser et al. 2001; Kucuktas et al. 2009). Even though a higher recombination rate in males was initially observed in Japanese flounder (Coimbra et al. 2003), this could not be validated in the second-generation linkage map for this species (Castano-Sanchez et al. 2010). In the present study, the female/male recombination ratio varied greatly among and within linkage groups, with the overall ratio being 0.86:1. Comparative Mapping

gilthead sea bream (Franch et al. 2006), tilapia (Lee et al. 2005), medaka (Naruse et al. 2000), and Japanese flounder (Castano-Sanchez et al. 2010; Coimbra et al. 2003). The estimated genome size of striped bass is about 900 Mb (Hinegard and Rosen 1972; Hardie and Hebert 2003, 2004), which results in an average ratio of about 554 Kb/cM. This ratio is similar to values for other fish species, such as zebrafish (Postlethwait et al. 1994) and yellowtail (Ohara et al. 2005). Twenty-six linkage groups were identified in this study. Since the haploid chromosome number of striped bass is 24 (Rachlin et al. 1978), we expect that, with the addition of more markers, some linkage groups will merge and the number of linkage groups will eventually match the haploid chromosome number. The linkage map is essential for many molecular genetics applications, such as mapping traits of interest,

Comparative mapping is a powerful genomic tool, which allows transfer of genomic information from well-studied model species to less-studied aquaculture species. A comparison of the striped bass linkage map to the stickleback genome revealed conserved synteny between these two species. Therefore, the genome sequence of stickleback can be used as a reference for targeted mapping of regions of interest in striped bass. Of the 480 markers screened for polymorphism in striped bass, 160 markers were monomorphic in these families and could not be placed onto the linkage map in this study. However, these markers might be polymorphic and useful in other mapping populations. Based on comparative information between striped bass and stickleback, we can postulate the putative map positions for these monomorphic markers with

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Table 2 Oxford plot between striped bass and three-spined stickleback

Striped bass

Stickleback Chromosome 2 13 11 19 5 15 1 1

?a LG1 3 LG2 5 1 LG3 13 1 LG4 5 1 0 LG5 2 3 LG6 7 4 LG7 6 1 0 LG8 11 0 LG9 10 0 LG10 5 2 0 LG11 5 1 LG12 1 8 0 LG13 3 2 LG14 3 1 0 LG15 7 0 LG16 9 0 LG17 5 0 LG18 5 0 LG19 4 0 LG20 1 4 0 LG21 3 0 LG22 3 0 LG23 2 2 LG24-26 1 1 1 0 The numbers of striped bass markers with significant hits against the stickleback genome are presented in the table, and the putative syntenic pairs are indicated by grey boxes 14 13

a

12

20 2

21

7

17

8

4

18

16

9

10

1

3

6

Scaffolds with unknown chromosomal locations

Fig. 2 Comparison of the striped bass sex-averaged linkage map with the assembled sequences of three-spined stickleback chromosome. The markers on striped bass linkage map are font-coded the same as in Fig. 1 and the map distances are in Kosambi cM. The three-spined stickleback chromosome is named with a prefix GAC (G. aculeatus). The positions (100 kb) of the sequences homologous to the markers on striped bass genetic map are presented on the right of the chromosome. More comparative maps are presented in (Additional file 5 of the “Electronic supplementary material”)

homologous sequences in stickleback. Moreover, it is even possible to identify candidate genes for traits of interest based on syntenic relationships. For example, candidate genes for infectious salmon anemia were identified based on comparative information between Atlantic salmon and model fish species (Li et al. 2011). However, caution should be used when using the genome sequence of stickleback as a reference. In spite of the highly conserved syntenic relationships between striped bass and stickleback at the chromosomal level, we observed complex colinearity within each chromosome. The level of conserved synteny is higher between species with closer phylogenetic distance. Both striped bass and European sea bass belong to the family Moronidae. Thus, highly conserved synteny between these two species is expected. In spite of the lack of a whole-genome sequence for either species, genomic resources for European sea bass are growing rapidly. Recently, 102,690 BACend sequences and 36,166 contigs assembled from wholegenome shotgun sequences have become available for European sea bass (Kuhl et al. 2010). We downloaded these sequences from GenBank and searched for homologous sequences using the sequence of the striped bass markers as queries (Additional file 6 of the “Electronic supplementary material”). As expected, homologous sequences were identified for some striped bass markers for which no homology had been observed in stickleback.

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Due to lack of a fully sequenced genome for both species, the syntenic relationships between striped bass and European sea bass can only be inferred indirectly. For example, European sea bass linkage group 4 shows homology to stickleback chromosome 8 (Guyon et al. 2010), which is also homologous with striped bass linkage group 7. Therefore, linkage group 7 of striped bass is likely to show homology to linkage group 4 of the European sea bass. Similarly, the homolgous relationships between striped bass and other species such as gilthead sea bream and tilapia can be inferred indirectly using stickleback as a “stepping stone”, as demonstrated by Sarropoulou and Fernandes (2010). Thus, the wealth of genomic resources developed in all these species can be used to facilitate mapping of traits of interest in striped bass. Acknowledgments The authors would like to thank Guangtu Gao for help with the software MULTIMAP, and Alanna MacIntyre and Georgeta Constantin for their technical assistance. We also thank Amber Garber, Mark Westerman, Andy McGinty, and Michael Hopper for help with marker and/or mapping family development. This project was funded by a Marine Aquaculture Initiative grant NAO60AR4170250 to CVS from the National Oceanic and Atmospheric Administration. The VIMS contribution number is 3180.

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