An integrated cytogenetic and physical map reveals unevenly distributed recombination spots along the papaya sex chromosomes

Chromosome Research

Volumn 20, Issue 6, 2012, Pages 753-767

  Wai, Ching Man ^a,b   Moore, Paul H ^b   Paull, Robert E ^a   Ming, Ray ^b,c   Yu, Qingyi ^b,d  

^a UNIVERSITY OF HAWAII   (United States)

^b HAWAII AGRICULTURE RESEARCH CENTER   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Carica papaya; Cytogeneticmap; Fluorescence in situ hybridization (FISH); Papaya chromosome 1; Sex chromosomes

Indexed keywords

ARTICLE; CENTROMERE; CHROMOSOME 1; CHROMOSOME ANALYSIS; CHROMOSOME ARM; CHROMOSOME MAP; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LOCATION; GENE LOCUS; GENETIC RECOMBINATION; HETEROCHROMATIN; MICROSATELLITE MARKER; NONHUMAN; PACHYTENE; PAPAYA; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEX CHROMOSOME; SEX LINKAGE; TELOMERE; X CHROMOSOME; Y CHROMOSOME;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BASE SEQUENCE; CARICA; CYTOGENETIC ANALYSIS; GENETIC MARKERS; IN SITU HYBRIDIZATION, FLUORESCENCE; MATRIX ATTACHMENT REGIONS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PHYSICAL CHROMOSOME MAPPING; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SEX CHROMOSOMES;

CARICA PAPAYA; CARICACEAE;

EID: 84868210757     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-012-9312-1     Document Type: Article

References (54)

1. Altinkut A, Kotseruba V, Kirzhner VM, Nevo E, Raskina O, Belyayev A (2006) Ac-like transposons in populations of wild diploid Triticeae species: Comparative analysis of chromosomal distribution. Chromosome Res 14:307-"317
2. Anderson LK, Lai A, Stack SM, Rizzon C, Gaut BS (2006) Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. Genome Res 16:115-"122
3. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, Westerman RP, Sanmiguel PJ, Bennetzen JL (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732
4. Blas AL, Yu Q, Chen C, Veatch O, Moore PH, Paull RE, Ming R (2009) Enrichment of a papaya high-density genetic map with AFLP markers. Genome/National Research Council Canada0Genome/Conseil national de recherches Canada 52:716-"725
5. Budiman MA, Chang SB, Lee S, Yang TJ, Zhang HB, de Jong H, Wing RA (2004) Localization of jointless-2 gene in the centromeric region of tomato chromosome 12 based on high resolution genetic and physical mapping. Theor Appl Genet 108:190-"196
6. Cermak T, Kubat Z, Hobza R, Koblizkova A, Widmer A, Macas J, Vyskot B, Kejnovsky E (2008) Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Res 16:961-"976
7. Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975-"997
8. Chen C, Yu Q, Hou S, Li Y, Eustice M, Skelton RL, Veatch O, Herdes RE, Diebold L, Saw J, Feng Y, Qian W, Bynum L, Wang L, Moore PH, Paull RE, Alam M, Ming R (2007) Construction of a sequence-tagged high-density genetic map of papaya for comparative structural and evolutionary genomics in brassicales. Genetics 177:2481-"2491
9. Cheng Z, Presting GG, Buell CR, Wing RA, Jiang J (2001) High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics 157:1749-"1757
10. Cheng Z, Buell CR, Wing RA, Jiang J (2002) Resolution of fluorescence in-situ hybridization mapping on rice mitotic prometaphase chromosomes, meiotic pachytene chromosomes and extended DNA fibers. Chromosome Res 10:379-"387
11. Choo KH (1998) Why is the centromere so cold? Genome Res 8:81-"82
12. Danilova TV, Birchler JA (2008) Integrated cytogenetic map of mitotic metaphase chromosome 9 of maize: Resolution, sensitivity, and banding paint development. Chromosoma 117:345-"356
13. Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, Quesneville H, Mezard C (2006) Variation in crossingover rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". Genome Res 16:106-"114
14. Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJ, Zabel P, de Jong JH (1996) High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J 9:421-"430
15. Gaut BS, Wright SI, Rizzon C, Dvorak J, Anderson LK (2007) Recombination: An underappreciated factor in the evolution of plant genomes. Nat Rev Genet 8:77-"84
16. Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang J (2008) Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics 180:1307-"1317
17. IRGSP (2005) The map-based sequence of the rice genome. Nature 436:793-"800
18. Jiang J, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome/National Research Council Canada0Genome/Conseil national de recherches Canada 49:1057-"1068
19. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462-"467
20. Kim JS, Islam-Faridi MN, Klein PE, Stelly DM, Price HJ, Klein RR, Mullet JE (2005a) Comprehensive molecular cytogenetic analysis of sorghum genome architecture: Distribution of euchromatin, heterochromatin, genes and recombination in comparison to rice. Genetics 171:1963-"1976
21. Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005b) Molecular cytogenetic maps of sorghum linkage groups 2 and 8. Genetics 169:955-"965
22. Koo DH, Jo SH, Bang JW, Park HM, Lee S, Choi D (2008) Integration of cytogenetic and genetic linkage maps unveils the physical architecture of tomato chromosome 2. Genetics 179:1211-"1220
23. Koumbaris GL, Bass HW (2003) A new single-locus cytogenetic mapping system for maize (Zea mays L.): Overcoming FISH detection limits with marker-selected sorghum (S. propinquum L.) BAC clones. Plant J 35:647-"659
24. Lambie EJ, Roeder GS (1986) Repression of meiotic crossing over by a centromere (CEN3) in Saccharomyces cerevisiae. Genetics 114:769-"789
25. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI, Zee FT, Paterson AH, Ming R (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348-"352
26. Ma H, Moore PH, Liu Z, Kim MS, Yu Q, Fitch MM, Sekioka T, Paterson AH, Ming R (2004) High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 166:419-"436
27. Matsuo M, Ito Y, Yamauchi R, Obokata J (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplastnuclear DNA flux. Plant Cell 17:665-"675
28. McClintock B (1929) Chromosome morphology in Zea mays. Science 69:629
29. Ming R, Moore PH, Zee FT, Abbey CA, Ma H, Paterson AH (2001) Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a treefruit genome. Theor Appl Genet 102:892-"899
30. Ming R, Wang J, Moore PH, Paterson AH (2007) Sex chromosomes in flowering plants. Am J Bot 94:141-"150
31. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL, Salzberg SL, Feng L, Jones MR, Skelton RL, Murray JE, Chen C, Qian W, Shen J, Du P, Eustice M, Tong E, Tang H, Lyons E, Paull RE, Michael TP, Wall K, Rice DW, Albert H, Wang ML, Zhu YJ, Schatz M, Nagarajan N, Acob RA, Guan P, Blas A, Wai CM, Ackerman CM, Ren Y, Liu C, Wang J, Wang J, Na JK, Shakirov EV, Haas B, Thimmapuram J, Nelson D, Wang X, Bowers JE, Gschwend AR, Delcher AL, Singh R, Suzuki JY, Tripathi S, Neupane K, Wei H, Irikura B, Paidi M, Jiang N, Zhang W, Presting G, Windsor A, Navajas- Perez R, Torres MJ, Feltus FA, Porter B, Li Y, Burroughs AM, Luo MC, Liu L, Christopher DA, Mount SM, Moore PH, Sugimura T, Jiang J, Schuler MA, Friedman V, Mitchell-Olds T, Shippen DE, dePamphilis CW, Palmer JD, Freeling M, Paterson AH, Gonsalves D, Wang L, Alam M (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991-"996
32. Miura A, Kato M, Watanabe K, Kawabe A, Kotani H, Kakutani T (2004) Genomic localization of endogenous mobile CACTA family transposons in natural variants of Arabidopsis thaliana. Mol Genet Genomics 270:524-"532
33. Nagarajan N, Navajas-Pérez R, Pop M, Alam M, Ming R, Paterson AH, Salzberg SL (2008) Genome-Wide Analysis of Repetitive Elements in Papaya Tropical Plant Biol 1:191-"201
34. Ouyang S, Buell CR (2004) The TIGR plant repeat databases: A collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res 32:D360-D363
35. Pedrosa-Harand A, Kami J, Gepts P, Geffroy V, Schweizer D (2009) Cytogenetic mapping of common bean chromosomes reveals a less compartmentalized small-genome plant species. Chromosome Res 17:405-"417
36. Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5:R79
37. Peters SA, Datema E, Szinay D, van Staveren MJ, Schijlen EG, van Haarst JC, Hesselink T, Abma-Henkens MH, Bai Y, de Jong H, Stiekema WJ, Klein Lankhorst RM, van Ham RC (2009) Solanum lycopersicum cv. Heinz 1706 chromosome 6: Distribution and abundance of genes and retrotransposable elements. Plant J 58:857-"869
38. Ren Y, Zhang Z, Liu J, Staub JE, Han Y, Cheng Z, Li X, Lu J, Miao H, Kang H, Xie B, Gu X, Wang X, Du Y, Jin W, Huang S (2009) An integrated genetic and cytogenetic map of the cucumber genome. PLoS One 4:e5795
39. Roberts PA (1965) Difference in the behavior of eu- and heterochromatin: Crossing-over. Nature 205:725-"726
40. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, GolserW, Kim H, Lee S, Lin J, Dujmic Z, KimW, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R,Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: Complexity, diversity, and dynamics. Science 326:1112-"1115
41. See DR, Brooks S, Nelson JC, Brown-Guedira G, Friebe B, Gill BS (2006) Gene evolution at the ends of wheat chromosomes. Proc Natl Acad Sci USA 103:4162-"4167
42. Sturtevant AH (1925) The effects of unequal crossing over at the bar locus in drosophila. Genetics 10:117-"147
43. Szinay D, Chang SB, Khrustaleva L, Peters S, Schijlen E, Bai Y, Stiekema WJ, van Ham RC, de Jong H, Klein Lankhorst RM (2008) High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome 6. Plant J 56:627-"637
44. Takata M, Kiyohara A, Takasu A, Kishima Y, Ohtsubo H, Sano Y (2007) Rice transposable elements are characterized by various methylation environments in the genome. BMC Genomics 8:469
45. Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141-"1160
46. Wai CM, Ming R, Moore PH, Paull RE, Yu Q (2010) Development of chromosome-specific cytogenetic markers and merging of linkage fragments in papaya. Trop Plant Biol 3:171-"181
47. Wang CJ, Harper L, Cande WZ (2006) High-resolution singlecopy gene fluorescence in situ hybridization and its use in the construction of a cytogenetic map of maize chromosome 9. Plant Cell 18:529-"544
48. Wright SI, Agrawal N, Bureau TE (2003) Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res 13:1897-"1903
49. Wu J, Mizuno H, Hayashi-Tsugane M, Ito Y, Chiden Y, Fujisawa M, Katagiri S, Saji S, Yoshiki S, Karasawa W, Yoshihara R, Hayashi A, Kobayashi H, Ito K, Hamada M, Okamoto M, Ikeno M, Ichikawa Y, Katayose Y, Yano M, Matsumoto T, Sasaki T (2003) Physical maps and recombination frequency of six rice chromosomes. Plant J 36:720-"730
50. Yu Q, Hou S, Feltus FA, Jones MR, Murray JE, Veatch O, Lemke C, Saw JH, Moore RC, Thimmapuram J, Liu L, Moore PH, Alam M, Jiang J, Paterson AH, Ming R (2008) Low X/Y divergence in four pairs of papaya sex-linked genes. Plant J 53:124-"132
51. Yu Q, Tong E, Skelton RL, Bowers JE, Jones MR, Murray JE, Hou S, Guan P, Acob RA, Luo MC, Moore PH, Alam M, Paterson AH, Ming R (2009) A physical map of the papaya genome with integrated genetic map and genome sequence. BMC Genomics 10:371
52. Zhang L, Gaut BS (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res 13:2533-"2540
53. Zhang W, Wang X, Yu Q, Ming R, Jiang J (2008) DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 18:1938-"1943
54. Zhang W, Wai CM, Ming R, Yu Q, Jiang J (2010) Integration of genetic and cytological maps and development of a pachytene chromosome-based karyotype in papaya. Trop Plant Biol 3:166-"170