Browse > Article

Association of A/T Rich Microsatellites with Responses to Artificial Selection for Larval Developmental Duration in the Silkworm Bombyx mori  

Pradeep, Appukuttan Nair Retnabhavan (Seribiotech Research Laboratory)
Awasthi, Arvind Kumar (Seribiotech Research Laboratory)
Urs, Raje Siddaraje (Seribiotech Research Laboratory)
Publication Information
Molecules and Cells / v.25, no.4, 2008 , pp. 467-478 More about this Journal
Abstract
Simple sequence repeats (SSRs) and interSSR (ISSR) marker systems were used in this study to reveal genetic changes induced by artificial selection for short/long larval duration in the tropical strain Nistari of the silkworm Bombyx mori. Artificial selection separated longer larval duration (LLD) ($29.428{\pm}0.723days$) and shorter larval duration (SLD) ($22.573{\pm}0.839days$) lines from a base, inbred population of Nistari (larval span of $23.143{\pm}0.35days$). SSR polymorphism was observed between the LLD and SLD lines at one microsatellite locus, Bmsat106 ($CA_7$) and at two loci of 1074 bp and 823 bp generated with the ISSR primer UBC873. Each of these loci was present only in the LLD line. The loci segregated in the third generation of selection and were fixed in opposite directions. In the $F_2$ generation of the $LLD{\times}SLD$ lines, the alleles of Bmsat106 and $UBC873_{1074bp}$ segregated in a 1:1 ratio and the loci were present only in the LLD individuals. $UBC873_{823bp}$ was homozygous. Single factor ANOVA showed a significant association between the segregating loci and longer larval duration. Together, the two alleles contributed to an 18% increase in larval duration. The nucleotide sequences of the $UBC873_{1074bp}$ and $UBC873_{823bp}$ loci had 67% A/T content and consisted of direct, reverse, complementary and palindromic repeats. The repeats appeared to be "nested" (59%) in larger repeats or as clustered elements adjacent to other repeats. Of 203 microsatellites identified, dinucleotides (67.8%) predominated and were rich in A/T and T/A motifs. The sequences of the $UBC873_{1074bp}$ and $UBC873_{823bp}$ loci showed similarity (E = 0.0) to contigs located in Scaffold 010774 and Scaffold 000139, respectively, of the B. mori genome. BLASTN analysis of the $UBC873_{1074bp}$ sequence showed significant homology of (nt.) 45-122 with upstream region of three exons from Bombyx. The complete sequence of this locus showed ~49% nucleotide conservation with transposon 412 of Drosophila melanogaster and the Ikirara insertions of Anopheles gambiae. The A + T richness and lack of coding potential of these small loci, and their absence in the SLD line, reflect the active process of genetic change associated with the switch to short larval duration as an adaptation to the tropics.
Keywords
Allele Segregation in $F_2$; AT Rich Microsatellites; Bombyx mori; Larval Duration; Loci-Trait Association; Selection;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 2  (Related Records In Web of Science)
연도 인용수 순위
1 Abbot, P. (2001). Individual and population variation in invertebrates revealed by inter-simple sequence repeats (ISSRs). J. Insect Sci. 1, 8.
2 Crow, J.F., and Kimura, M. (1970). An Introduction to Population Genetics Theory. (Minneapolis, USA: Burgess Publishing)
3 Daborn, P.J., Yen, J.L., Bogwitz, M.R., Le Goff G., Feil, E., Jeffers, S., Tijet, N., Perry, T., Heckel, D., Batterham, P., et al. (2002). A single p450 allele associated with insecticide resistance in Drosophila. Science 297, 2253-2256   DOI   ScienceOn
4 Deshpande, A.U., Apte, G.S., Bahulikar, R.A., Lagu, M.D., Kulkarni, B.G., Suresh, H.S., Singh, N.P., Rao, M.K., Gupta, V.S., Pant, A., et al. (2001). Genetic diversity across natural populations of three montane plant species from the Western Ghats, India revealed by inter simple sequence repeats. Mol. Ecol. 10, 2397-2408   DOI   ScienceOn
5 Gage, L.P. (1974). The Bombyx mori genome analysis by DNA reassociation kinetics. Chromosoma 45, 27-42
6 Holland, J.B., Helland, S.J., Sharopova, N., and Rhyne, D.C. (2001). Polymorphism of PCR-based markers targeting exons, introns, promoter regions, and SSRs in maize and introns and repeat sequences in oat. Genome 44, 1065-1076   DOI
7 Keightley, P.D. (1998). Genetic basis of response to 50 generations of selection on body weight in inbred mice. Genetics 148, 1931-1939
8 Kurtz, S., Choudhuri, J.V., Ohlebusch, E., Schleiermacher, C., Stoye, J., and Giegerich, R. (2001). REPuter: The manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29, 4633-4642   DOI   ScienceOn
9 Mackay, T.F.C., Lyman, R.F., and Lawrence, F. (2005). Polygenic mutation in Drosophila melanogaster: Mapping spontaneous mutations affecting sensory bristle number. Genetics 170, 1723-1735   DOI   ScienceOn
10 Masidae, X., Bartolome, C., and Charlsworth, B. (2002). S-element insertions are associated with the evolution of the Hsp70 genes in Drosophila melanogaster. Curr. Biol. 12, 1686-1691   DOI   ScienceOn
11 Mita, K., Kasahara, M., Sasaki, S., Nagayasu, Y., Yamada, T., Kanamori, H., Namiki, N., Kitagawa, M., Yamashita, H., Yasukochi, Y., et al. (2004). The genome sequence of silkworm, Bombyx mori. DNA Res. 11, 27-35   DOI
12 Mukherjee, N.G. (1912). Handbook of Sericulture, Government Book Depot, Calcutta, India
13 Pradeep, A.R., Anuradha, H. J., and Raje Urs, S. (2007). Molecular markers for biomass traits: association, interaction and genetic divergence in silkworm, Bombyx mori. Biomarker Insights 2, 197-217, available online
14 Prasad, M.D., Muthulakshmi, M., Madhu, M., Archak, S., Mita, K., and Nagaraju, J. (2005). Survey and analysis of microsatellites in the silkworm, Bombyx mori: frequency, distribution, mutations, marker potential and their conservation in heterologous species. Genetics 169, 197-214   DOI   ScienceOn
15 Rizzon, C., Martin, E., Marais, G., Duret, L., Segalat, L., and Biemont, C. (2003). Patterns of selection against transposons inferred from the distribution of Tc1, Tc3 and Tc5 insertions in the mut-7 line of the nematode Caenorhabditis elegans. Genetics 165, 1127-1135
16 Robertson, H.M. (2002). Evolution of DNA transposons in eukaryotes. In Mobile DNA II, N.L. Craig, R. Craige, and A.M. Lambowitz, eds. (Washington DC, USA: ASM Press)
17 Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (NY, USA: Cold Spring Harbor Laboratory Press)
18 Scheiner, S.M. (2002). Selection experiments and the study of phenotypic plasticity. J. Evol. Biol. 15, 889-898   DOI   ScienceOn
19 Schlotterer, C. (2000). Evolutionary dynamics of microsatellite DNA. Chromosoma 109, 365-371   DOI
20 Schnabel, R.D., Taylor, J.F., and Derr, J.N. (2003). Development of a linkage map and QTL scan for growth traits in North American bison. Cytogenet. Genome Res. 102, 59-64   DOI   ScienceOn
21 Toth, G., Gaspari, Z., and Jurka, J. (2000). Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res. 10, 967-981   DOI
22 Li, Y.-C., Korol, A.B., Fahima, T., Beiles, A., and Nevo, E. (2002). Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 11, 2453-2465   DOI   ScienceOn
23 Hong, C.P., Piao, Z.Y., Kang, T.W., Batley, J., Yang, T.J., Hur, Y.K., Bhak, J., Park, B.S., Edwards, D., and Lim, Y.P. (2007). Genomic distribution of simple sequence repeats in Brassica rapa. Mol. Cells 23, 349-356
24 Vijayan, K., Anuradha, H.J., Nair, C.V., Pradeep, A.R., Awasthi, A.K., Saratchandra, B., Rahman, S.A.S., Singh, K.C., Chakraborti, R., and Urs, S. Raje. (2006). Genetic diversity and differentiation among populations of the Indian eri silkworm, Samia cynthia ricini, revealed by ISSR markers. J. Insect Sci. 6, available online: insectscience.org/6.30
25 Nagaraju, J., Kathirvel, M., Muthulakshmi, M., Subbiah, E.V., and Kumar, L.D. (2002). FISSR-PCR: a simple and sensitive assay for high throughput genotyping and genetic mapping. Mol. Cell. Probes 16, 67-72   DOI   ScienceOn
26 Franchini, L.F., Ganko, E.W., and McDonald, J.F. (2004). Retrotransposon- gene associations are wide-spread among D. melanogaster populations. Mol. Biol. Evol. 21, 1323-1331   DOI   ScienceOn
27 Reddy, K.D., Nagaraju, J., and Abraham, E.G. (1999b). Genetic characterization of silkworm Bombyx mori by simple sequence repeats (SSR) - anchored PCR. Heredity 83, 681-687   DOI   ScienceOn
28 Hill, S.R., Leung, S.S., Quercia, N.L., Vasiliauskas, D., Yu, J., Pasic, I., Leung, D., Tran, A., and Romans, P. (2001). Ikirara insertions reveal five new Anopheles gambiae transposable elements in islands of repetitious sequence. J. Mol. Evol. 52, 215-231   DOI
29 Nagaraju, J., and Goldsmith, M.R. (2002). Silkworm genomics - progress and prospects. Curr. Sci. 83, 415-425
30 Yoshida, T., Ohkumo, T., Ishibashi, S., and Yasuda, K. (2005). The 50-AT-rich half-site of Maf recognition element: a functional target for bZIP transcription factor Maf. Nucleic Acids Res. 33, 3465-3478   DOI   ScienceOn
31 Pasyukova, E.G., Nuzhdin, S.V., Morozova, T.V., and Mackay, T.F.C. (2004). Accumulation of transposable elements in the genome of Drosophila melanogaster is associated with a decrease in fitness. J. Heredity 95, 284-290   DOI   ScienceOn
32 Kaminker, J.S., Bergman, C.M., Kronmiller, B., Carlson, J., Svirskas, R., Patel, S., Frise, E., Wheeler, D.A., Lewis, S.E., Rubin, G.M., et al. (2002). The transposable elements of the Drosophila melanogaster euchromatin: a genomic perspective. Genome Biol. 3, Research0084
33 Murakami, A., and Imai, H. (1974). Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina (Bombycidae, Lepiodoptera). Chromosoma 47, 167-178   DOI
34 Jankowski, C., Naser, F., and Nag, D.K. (2000). Meiotic instability of CAG repeat tracts occurs by double-strand break repair in yeast. Proc. Natl. Acad. Sci. USA 97, 2134-2139
35 Korpelainen, H., Kostamo, K., and Virtanen, V. (2007). Microsatellite marker identification using genome screening and restriction-ligation. Biotechniques 42, 479-486   DOI
36 Fu, H., Park, W., Yan, X., Zheng, Z., Shen, B., and Dooner, H.K. (2001). The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc. Natl. Acad. Sci. USA 98, 8903-8908
37 Strand, M., Prolla, T.A., Liskay, R.M., and Petes, T.D. (1993). Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch pair. Nature 365, 274-276   DOI   ScienceOn
38 Cortese, M.D., Norry, F.M., Piccinali, R., and Hasson, E. (2002). Direct and correlated responses to artificial selection on developmental time and wing length in Drosophila buzzatii. Evolution Int. J. Org. Evolution 56, 2541-2547   DOI
39 Ganko, E.W., Greene, C.S., Lewis, J.A., Bhattacharjee, V., and McDonald, J.F. (2006). LTR retrotransposon-gene associations in Drosophila melanogaster. J. Mol. Evol. 62, 111-120   DOI
40 Baker, R.E., and Rogers, K. (2005). Genetic and genomic analysis of the AT-rich centromere DNA element II of Saccharomyces cerevisiae. Genetics 171, 1463-1475   DOI   ScienceOn
41 Tu, Z. (2001). Eight novel families of miniature inverted repeat transposable elements in the African malaria mosquito, Anopheles gambiae. Proc. Natl. Acad. Sci. USA 98, 1699-1704
42 Norris, D.E., Shurtleff, A.C., Toure, Y.T., and Lanzaro, G.C. (2001). Microsatellite DNA polymorphism and heterozygosity among field and laboratory populations of Anopheles gambiae s.s (Diptera: Culicidae). J. Med. Entomol. 38, 336-340   DOI   ScienceOn
43 McCollum, A.M., Ganko, E.W., Barrass, P.A., Rodriguez, J.M., and McDonald, J.F. (2002). Evidence for the adaptive significance of an LTR retrotransposon sequence in a Drosophila heterochromatic gene. BMC Evol. Biol. 2, 5   DOI
44 Keightley, P.D., and Ohnishi, O. (1998). EMS-induced polygenic mutation rates for nine quantitative characters in Drosophila melanogaster. Genetics 148, 753-766
45 Mitchell-Olds, T., and Schmitt, J. (2006). Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947-952   DOI   ScienceOn
46 Reddy, K.D., Abraham, E.G., and Nagaraju, J. (1999a). Microsatellites of the silkworm, Bombyx mori: abundance, polymorphism and strain characterization. Genome 42, 1057-1065   DOI
47 Ellegren, H. (2004). Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5, 435-445   DOI   ScienceOn
48 Witherspoon, D.J., Doak, T.G., Wiliams, K.R., Seegmiller, A., Serger, J., and Herrick, G. (1997). Selection on the protein - coding genes of the TBE I family of transposable elements in the ciliates Oxytricha fallax and O. trifallax. Mol. Biol. Evol. 14, 696-706   DOI   ScienceOn
49 Churchill, M.E., and Suzuki, M. (1989). 'SPKK' motifs prefer to bind to DNA at A/T-rich sites. EMBO J. 8, 4189-4195
50 Deka, J., Herter, P., Sprenger-Haubels, M., Koosch, S., Franz, D., Muller, K.-M., Kuhnen, C, Hofmann, I., and Muller, O. (1999). The APC protein binds to A/T rich DNA sequences. Oncogene 18, 5654-5661   DOI
51 Sreenu, V.B., Kumar, P., Nagaraju, J., and Nagarajaram, H.A. (2007). Simple sequence repeats in mycobacterial genomes. J. Biosci. 32, 3-15   DOI
52 Witten, J.T., Chen, C.T.L., and Cohen, B.A. (2007). Complex genetic changes in strains of Saccharomyces cerevisiae derived by selection in the laboratory. Genetics 117, 449-456
53 Mackay, T.F.C., Fry, J.D., Lyman, R.F., and Nuzhdin, S.V. (1994). Polygenic mutation in Drosophila melanogaster: estimates from response to selection in inbred strains. Genetics 136, 937-951
54 zur Lage, P., Shrimpton, A.D., Flavell, A.J., Mackay, T.F.C., and Brown, A.J. (1997). Genetic and molecular analysis of smooth, a quantitative trait locus affecting bristle number in Drosophila melanogaster. Genetics 146, 607-618
55 Ashley, C.T., Pendleton, C.G., Jennings, W.W., Sexana, A., and Glover, C.V.C. (1989). Isolation and sequencing of cDNA clones encoding Drosophila chromosomal protein D1. A repeating motif in proteins which recognize at DNA. J. Biol. Chem. 264, 8394-8401
56 Lyman, R.F., Lawrence, F., Nuzhdin, S.V., and Mackay, T.F.C. (1996). Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics 143, 277-292
57 Robertson, H.M., and Zumpano, K.L. (1997). Molecular evolution of an ancient mariner transposon, Hsmar I, in the human genome. Gene 205, 203-217   DOI   ScienceOn
58 Goldsmith, M.R., Shimada, T., and Abe, H. (2005). The genetics and genomics of the silkworm, Bombyx mori. Ann. Rev. Entomol. 50, 71-100   DOI   ScienceOn
59 Regelson, M., Eller, C.D., Horvath, S., and Marahrens, Y. (2006). A link between repetitive sequences and gene replication time. Cytogenet. Genome Res. 112, 184-193   DOI   ScienceOn
60 Miao, X.X., Xub, S.J., Li, M.H., Li, M.W., Huang, J.H., Dai, F.Y., Marino, S.W., Mills, D.R., Zeng, P., Mita, K., et al. (2005). Simple sequence repeat-based consensus linkage map of Bombyx mori. Proc. Natl. Acad. Sci. USA 102, 16303-16308
61 Ichimura, S., and Mita, K. (1992). Essential role of duplications of short motif sequences in the genomic evolution of Bombyx mori. J. Mol. Evol. 35, 123-130
62 Kruglyak, S., Durrett, R.T., Schug, M.D., and Aquadro, C.F. (1998). Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc. Natl. Acad. Sci. USA 95, 10774-10778
63 Udupa, S.M., Weigand, F., Saxena, M.C., and Kahl, G. (1998). Genotyping with RAPD and microsatellite markers resolves pathotype diversity in the ascochyta blight pathogen of chick pea. Theor. Appl. Genet. 97, 299-307   DOI
64 Azevedo, R.B.R., Keightley, P.D., Laurén-Maatta, C., Vassilieva, L.L., Lynch, M., and Leroi, A.M. (2002). Spontaneous mutational variation for body size in Caenorhabditis elegans. Genetics 162, 755-765
65 Nagaraju, J., Klimenko, V., and Couble, P. (2000). The silkworm, Bombyx mori: A model genetic system. In Encyclopedia of Genetics, E. Reeves, ed. (London, UK: Fitzroy Dearborn), pp. 219-239
66 Weber, J.L. (1990). Informativeness of human $(dC-dA)_n.\;(dG-dT)_n$ polymorphisms. Genomics 7, 524-530   DOI
67 Xia, Q., Zhou, Z., Lu, C., Cheng, D., Dai, F., Li, B., Zhao, P., Zha, X., Cheng, T., Chai, C., et al. (2004). A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306, 1937-1940   DOI   ScienceOn
68 Xiang, Z.H. (1995). Genetics and breeding of the silkworm. (Beijing, China: Chinese Agriculture Press), pp. 273-289
69 Pradeep, A.R., Chatterjee, S.N., and Nair, C.V. (2005). Genetic differentiation induced by selection in an inbred population of the silkworm Bombyx mori revealed by RAPD and ISSR marker systems. J. Appl. Genet. 46, 291-298
70 Suzuki, Y., Gage, L., and Brown, D.D. (1972). The genes for silk fibroin in Bombyx mori. J. Mol. Biol. 70, 637-649   DOI
71 Zietkiewicz, E., Rafalski, A., and Labuda, D. (1994) Genome fingerprinting by simple sequence repeat (SSR) - anchored polymerase chain reaction amplification. Genomics 20, 176-183   DOI   ScienceOn
72 Tu, Z. (2000). Molecular and evolutionary analysis of two divergent subfamilies of a novel miniature inverted repeat transposable element in the yellow fever mosquito, Aedes aegypti. Mol. Biol. Evol. 17, 1313-1325   DOI   ScienceOn
73 Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402   DOI
74 Ehtesham, N.Z., Bentur, J.S., and Bennett, J. (1995). Characterization of a DNA sequence that detects repetitive DNA elements in the Asian gall midge (Orseolia oryzae) genome: Potential use in DNA fingerprinting of biotypes. Gene 153, 179-183   DOI   ScienceOn