Evidence of allopolyploidy in urochloa humidicola based on cytological analysis and genetic linkage mapping

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Vigna, Bianca B Z ^a,b   Santos, Jean C S ^a   Jungmann, Leticia ^b,f   Valle, Cacilda B Do ^b   Mollinari, Marcelo ^c   Pastina, Maria M ^d   Pagliarini, Maria Suely ^e   Garcia, Antonio A F ^c   Souza, Anete P Souza ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b EMBRAPA CERRADOS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d EMBRAPA MILHO E SORGO   (Brazil)

^e STATE UNIVERSITY OF MARINGÁ   (Brazil)

^f Department of Genetics and Cell Biology ^*  (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPOLYPLOIDY; ANAPHASE; APOMIXIS; BRACHIARIA; CULTIVAR; FORAGE; GENETIC LINKAGE; GENETIC RESOURCE; GENOME; GRASS; HEXAPLOIDY; MEIOSIS; METAPHASE; MICROSATELLITE MARKER; NUCLEOLUS; QUANTITATIVE TRAIT LOCUS; SIMPLE SEQUENCE REPEAT; SPECIES; TROPICS; UROCHLOA; GENETICS; POACEAE; POLYPLOIDY;

MICROSATELLITE DNA;

GENETIC LINKAGE; MEIOSIS; MICROSATELLITE REPEATS; POACEAE; POLYPLOIDY;

EID: 84977605605     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0153764     Document Type: Article

References (91)

1. Keller-Grein G, Maass BL, Hanson J. (1996) Natural variation in Brachiaria and existing germplasm collections. In: Miles JW, Maass BL, Valle CB do (Eds.) Brachiaria: biology, agronomy and improvement. Brasília: Embrapa: /CIAT, Cali, pp 16-42.
2. Valle CB do & Savidan YH. (1996) Genetics, cytogenetics and reproductive biology of Brachiaria. In: Miles JW, Maass BL, Valle CB do (Ed.) Brachiaria: biology, agronomy and improvement. Brasília: Embrapa; Cali:CIAT,. pp. 147-163.
3. Jungmann L, Vigna BBZ, Paiva J, Sousa ACB, Valle CB, Laborda PR, Zucchi MI, Souza AP. Development of microsatellite markers for Brachiaria humidicola (Rendle) Schweick. Conservation Genet Res. 2009; 1: 475-479. doi: 10.1007/s12686-009-9111-y
4. Miles JW, Escandon ML. Further evidence on the inheritance of reproductive mode in Brachiaria. Can J Plant Sci. 1997; 77: 105-107.
5. Pessino SC, Ortiz J, Leblanc O, do Valle CB, Hayward MD. Identification of a maize linkage group related to apomixis in Brachiaria. Theor Appl Gen. 1997; 94:439-44.
6. Pessino SC, Evans C, Ortiz JPA, Armstead I, do Valle CB, Hayward MD. A genetic map of the apospory-region in Brachiaria hybrids: identification of two markers closely associated with the trait. Hereditas. 1998; 128: 153-58.
7. Adamowski E de V, Boldrini KR, Pagliarini MS, Valle CB do. Abnormal cytokinesis in microsporogenesis of Brachiaria humidicola (Poaceae: Paniceae). Gen. Mol. Res. 2007; 6: 616-621.
8. Boldrini KR, Pagliarini MS, Valle CB. Meiotic behavior of a nonaploid accession endorses x = 6 for Brachiaria humidicola (Poaceae). Gen Mol Res. 2009a; 8:1444-1450.
9. Boldrini KR, Micheletti PL, Gallo PH, Mendes-Bonato AB, Pagliarini MS, Valle CB. Origin of a polyploid accession of Brachiaria humidicola (Poaceae: Panicoideae: Paniceae). Gen Mol Res. 2009; 8: 888-895.
10. Boldrini KR, Pagliarini MS, Valle CB do. Evidence of natural hybridization in Brachiaria humidicola (Rendle) Schweick. (Poaceae: Panicoideae: Paniceae). J of Genet. 2010; 89: 91-94.
11. de Penteado MIO, dos Santos ACM, Rodrigues IF, do Valle CB, Seixas MAC, Esteves A. (2000) Determinação de ploidia e avaliação da quantidade de DNA total em diferentes espécies do gênero Brachiaria. Campo Grande: Embrapa Gado de Corte.
12. Ishigaki G, Gondo T, Ebina M, Suenaga K, Akashi R. Estimation of genome size in Brachiaria species. Japanese Society of Grassland Science. 2010; 56: 240-242.
13. Bernini C, Marin-Morales A. Karyotype analysis in Brachiaria (Poaceae) species. Cytobios. 2001; 104: 157-171. PMID: 11318511
14. Mendes DV, Boldrini KR, Mendes-Bonato AB, Pagliarini MS, Valle CB do. Cytological evidence of natural hybridization in Brachiaria brizantha Stapf (Gramineae). Bot J Linn Soc. 2006; 150: 441-446.
15. Boldrini KR, Pagliarini MS, Valle CB do. Abnormal timing of cytokinesis in microsporogenesis in Brachiaria humidicola (Poaceae: Paniceae). Jf Gen. 2006; 85: 225-228.
16. Nielen S, Almeida LM, Carneiro VTC, Araujo ACG. Physical mapping of rDNA genes corroborates allopolyploid origin in apomictic Brachiaria brizantha. Sex Plant Reprod. 2010; 23: 45-51. doi: 10.1007/ s00497-009-0124-1 PMID: 20165963
17. Risso-Pascotto C, Mendes DV, Silva N, Pagliarini MS, Valle CB. Evidence of allopolyploidy in Brachiaria brizantha (Poaceae: Paniceae) through chromosome arrangement at metaphase plate during microsporogenesis. Gen Mol Res. 2006; 5: 797-803.
18. Gallo PH, Micheletti PL, Boldrini KR, Risso-Pascotto C, Pagliarini MS, Valle CB do. 2n Gamete formation in the genus Brachiaria (Poaceae:Paniceae). Euphytica. 2008; 154: 255-260.
19. Ripol MI, Churchill GA, Da Silva JAG, Sorrells M. Statistical aspects of genetic mapping in autopolyploids. Gene. 1999; 235: 31-41. PMID: 10415330
20. Wu KK, Burnquist W, Sorrells ME, Tew TL, Moore PH, Tanksley SD. The detection and estimation of linkage in polyploids using single-dose restriction fragments. Theor and Appl Gen. 1992; 83: 294-300.
21. Da Silva JAG, Sorrells ME, Burnquist WL, Tanksley SD. RFLP linkage map and genome analysis of Saccharum spontaneum. Genome. 1993; 36: 782-791. PMID: 18470024
22. Ming R, Liu SC, Lin YR, Da Silva J, Wilson W, Braga D, van Deynze A, Wenslaff TF, Wu KK, Moore PH, Burnquist W, Sorrells ME, Irvine JE, Paterson AH. Detailed alignment of Saccharum and Sorghum chromosomes: comparative organization of closely related diploid and polyploid genomes. Genetics. 1998; 150: 1663-1682. PMID: 9832541
23. Al Janabi SM, Honeycutt RJ, McClelland M, Sobral BWS. A genetic linkage map of Saccharum spontaneum L. 'SES 208'. Genetics. 1993; 134: 1249-1260. PMID: 8375659
24. Porceddu A, Albertini E, Barcaccia E, Falistocco E, Falcinelli M. Linkage mapping in apomictic and sexual Kentucky bluegrass (Poa pratensis L.) genotypes using a two way pseudo-testcross strategy based on AFLP and SAMPL markers. Theor Appl Gen. 2002; 104: 273-280.
25. Jessup RW, Burson BL, Burrow G, Wang YW, Chang C, Li Z, Paterson AH, Hussey MA. Segmental allotetraploidy and allelic interactions in buffelgrass (Pennisetum ciliare (L.) Link syn. Cenchrus ciliaris L) as revealed by genome mapping. Genome. 2003; 46: 304-313. PMID: 12723046
26. Saha MC, Mian R, Zwonitzer JC, Chekhovskiy K, Hopkins AA. An SSR and AFLP based genetic linkage map of tall fescue (Festuca arundinacea Schreb.). Theor Appl Gen. 2005; 110: 323-336.
27. Ebina M, Nakagawa H, Yamamoto T, Araya H, Tsuruta S, Takahra M, Nakayima K. Co-segregation of AFLP and RAPD markers to apospory in Guineagrass (Panicum maximum Jacq.). Grassland Sci. 2005; 51: 71-78.
28. Bethel CM, Sciara EB, Estill JC, Bowers JE, Hanna W, Paterson AH. A framework map of bermudagrass (Cynodon dactylon x transvaalensis) based on single-dose restriction fragments. Theor Appl Gen. 2006; 112: 727-737.
29. Stein J, Pessino SC, Martínez EJ, Rodriguez MP, Siena LA, Quarin CL, Ortiz JPA. A genetic map of tetraploid Paspalum notatum Flügge (bahiagrass) based on single-dose molecular markers. Mol Breeding. 2007; 20:153-166.
30. Oliveira KM, Pinto LR, Marconi TG, Margarido GRA, Pastina MM, Teixeira LHM, Figueira AV, Ulian EC, Garcia AAF, Souza AP. Functional integrated genetic linkage map based on ESTmarkers for a sugarcane (Saccharum spp.) commercial cross. Mol Breeding. 2007; 20: 189-208.
31. Garcia AA, Kido EA, Meza AN, Souza HM, Pinto LR, Pastina MM, Leite CS, Silva JA, Ulian EC, Figueira A, Souza AP. Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theoretical and Applied Genetics. 2006; 112: 298-314. PMID: 16307229
32. Okada M, Lanzatella C, Saha MC, Bouton J, Wu R, Tobias CM. Complete Switchgrass Genetic Maps Reveal Subgenome Collinearity, Preferential Pairing and Multilocus Interactions. Genetics. 2010; 185: 745-760. doi: 10.1534/genetics.110.113910 PMID: 20407132
33. Maliepaard C, Jansen J, Van-Ooijen JW. Linkage analysis in a full-sib family of an outbreeding plant species: overview and consequences for applications. Genet Res. 1997; 70: 237-250.
34. Ozias-Akins P, Roche D, Hanna WW. Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus which may have no allelic form in sexual genotypes. Proc. Natl. Acad. Sci. USA. 1998; 95: 5127-5132.PMID: 9560240
35. Ozias-Akins P, Akiyama Y, Hanna WW. Molecular characterization of the genomic region linked with apomixis in Pennisetum/Cenchrus. Funct and Integr Gen. 2003; 3: 94-104.
36. Akiyama Y, Hanna WW, Ozias-Akins P. High-resolution physical mapping reveals that the aposporyspecific genomic region (ASGR) in Cenchrus ciliaris is located on a heterochromatic and hemizygous region of a single chromosome. Theoretical and Applied Genetics. 2005; 111: 1042-1051. PMID: 16133318
37. Goel S, Chen Z, Akiyama Y, Conner JÁ, Basu M, Gualtieri G, Hanna WW, Ozias-Atkins P. Comparative Physical mapping of the apospory-specific genomic region in two apomictic grasses: Pennisetum squamulatum and Cenchrus ciliaris. Genetics. 2006; 173: 389-400. PMID: 16547108
38. Gualtieri G, Conner JÁ, Morishige DT, Moore LD, Mullet JE, Ozias-Atkins P. A segment of the apospory-specific genomic region is highly microsyntenic not only between the apomicts Pennisetum squamulatum and buffelgrass, but also with a Rice chromosome 11 centromeric-proximal genomic region. Plant Physiol. 2006; 140: 963-971. PMID: 16415213
39. Conner JA, Goel S, Gunawan G, Cordonnier-Pratt MM, et al. Sequence analysis of bacterial artificial chromosome clones from the apospory-specific genomic region of Pennisetum and Cenchrus. Plant physiol. 2008; 147(3): 1396-411. doi: 10.1104/pp.108.119081 PMID: 18508959
40. Huo H, Conner JA, Ozias-Akins P. Genetic mapping of the apospory-specific genomic region in Pennisetum squamulatum using retrotransposon-based molecular markers. Theor Appl Genetics. 2009; 119: 199-212. doi: 10.1007/s00122-009-1029-y
41. Zorzatto C, Chiari L, Bitencourt GA, Valle CB, Leguizamón GOC, Schuster I, Pagliarini MS. Identification of a molecular marker linked to apomixis in Brachiaria humidicola (Poaceae). Plant Breeding. 2010; 129: 734-736. doi: 10.1111/j.1439-0523.2010.01763.x
42. Chiari L, Bitencourt G de A, Salgado LR, Valle CB, Leguizamon GOC. Identificação precoce de híbridos de Brachiaria humidicola por marcadores moleculares. In: Anais do Simpósio Internacional Sobre Melhoramento de Forrageira, Campo Grande, MS, 2007. Campo Grande: EMBRAPA CNPGC, 2007. p.1-3.
43. Jungmann L, Vigna BBZ, Boldrini KR, Sousa ACB, Valle CB, Resende RMS, Pagliarini MS, Zucchi MI, Souza AP. Genetic diversity and population structure analysis of the tropical pasture grass Brachiaria humidicola based on microsatellites, cytogenetics, morphological traits, and geographical origin. Genome. 2010; 53: 698-709. doi: 10.1139/g10-055 PMID: 20924419
44. Ricci GL, Souza-Kaneshima AM, Pagliarini MS, Valle CB. Meiotic behavior in Brachiaria humidicola (Poaceae) hybrids. Euphytica. 2011; 182: 355-361.
45. Bitencourt GA, do Valle CB, Chiari L, Salgado LR. Análise do modo de reprodução e determinação de híbridos por RAPD em Brachiaria humidicola. In: Anais do 54° Congresso Brasileiro de Genética, 2007; Águas de Lindóia. Anais. Ribeirão Preto: SBG, 2007
46. do Valle CB, Bitencourt GA, Chiari L, Resende RMS, Jank L, Arce AQ. Identification of the mode of reproduction in Brachiaria humidicola hybrids. In: International Congress on Sexual Plant Reproduction, 20, 2008, Brasília . Brasília: Embrapa Recursos Genéticos e Biotecnologia, 2008. p. 197-197.
47. Hoarau JY, Grivet L, Offmann B, D'Hont A, Risterucci AM, Roques D, Glaszmann JC, Grivet L. Genetic dissection of a modern sugarcane cultivar (Saccharum spp.) I. Genome mapping with AFLP markers. Theor Appl Genet. 2001; 103: 84-97.
48. Mollinari M, Silva RR, Margarido GRA, Oliveira KM, Marconi TG, Souza AP, Garcia AAF. (2009) Development of an integrated genetic linkage map of sugarcane (Saccharum spp.) incorporating double and triple dose markers. Resumos do 55° Congresso Brasileiro de Genética. Águas de Lindóia, 2009. ISBN 978-85-89109-06-2.
49. Aitken KS, Jackson PA, McIntyre CL. Construction of a genetic linkage map of Saccharum officinarum incorporating both simplex and duplex markers to increase genome coverage. Genome. 2007; 50: 742-756. PMID: 17893734
50. Cervantes-Flores JC, Yencho GC, Kriegner A, Pecota KV, Faulk MA, Mwanga ROM, Sosinski BR. Development of a genetic linkage map and identification of homologous linkage groups in sweetpotato using multiple-dose AFLP markers. Mol Breeding. 2008; 21:511-532.
51. Leach LJ, Wang L, Kearsey MJ, Luo Z. Multilocus tetrasomic linkage analysis using hidden Markov chain model. P. Natl. Acad. Sci. USA. 2010; 107: 4270-4274.
52. Hackett CA, McLean K, Bryan GJ. Linkage Analysis and QTL Mapping Using SNP Dosage Data in a Tetraploid Potato Mapping Population. PLoS ONE. 2013; 8: e63939. doi: 10.1371/journal.pone.0063939 PMID: 23704960
53. Garcia AAF, Mollinari M, Marconi TG, Serang OR, Silva RR, Vieira MLC, Vicentini R, Costa EA, Mancini MC, Garcia MOS, Pastina MM, Gazaffi R, Martins ERF, Dahmer N, Sforça DA, Silva CBC, Bundock P, Henry RJ, Souza GM, van Sluys MA, Landell MGA, Carneiro MS, Vincentz MAG, Pinto LR, Vencovsky R, Souza AP. SNP genotyping allows an in-depth characterization of the genome of sugarcane and other complex autopolyploids. Scientific Reports. 2013; 3: 3399. doi: 10.1038/srep03399 PMID: 24292365
54. Byers RL, Harker DB, Yourstone SM, Maughan PJ, Udall JA. Development and mapping of SNP assays in allotetraploid cotton. Theor Appl Genet. 2012; 124:1201-1214. doi: 10.1007/s00122-011-1780-8 PMID: 22252442
55. Clevenger J, Chavarro C, Pearl SA, Ozias-Akins P, Jackson SA. Single Nucleotide Polymorphism Identification in Polyploids: A Review, Example, and Recommendations. Molecular Plant. 2015; 8: 831-846. doi: 10.1016/j.molp.2015.02.002 PMID: 25676455
56. Rife TW, Wu S, Bowden RL, Poland JA. Spiked GBS: a unified, open platform for single marker genotyping and whole-genome profiling. BMC Genomics. 2015; 16:248. doi: 10.1186/s12864-015-1404-9PMID: 25880848
57. Serang O, Mollinari M, Garcia AAF. Efficient Exact Maximum a Posteriori Computation for Bayesian SNP Genotyping in Polyploids. PLoS ONE. 2012; 7: e30906. doi: 10.1371/journal.pone.0030906PMID: 22363513
58. Uitdewilligen JGAML, Wolters A-MA, D'hoop BB, Borm TJA, Visser RGF, et al. A Next-Generation Sequencing Method for Genotyping-by-Sequencing of Highly Heterozygous Autotetraploid Potato. PLoS ONE. 2013; 8: e62355. doi: 10.1371/journal.pone.0062355 PMID: 23667470
59. Solberg TR, Sonesson AK, Woolliams JA, Meuwissen THE. Genomic selection using different marker types and densities. J. Anim. Sci. 2008; 86:2447-2454. doi: 10.2527/jas.2007-0010 PMID: 18407980
60. Miller JM, Malenfant RM, David P, Davis CS, Poissant J, Hogg JT, Festa-Bianchet M, Coltman DW. Estimating genome-wide heterozygosity: effects of demographic history and marker type. Heredity. 2014; 112: 240-247. doi: 10.1038/hdy.2013.99 PMID: 24149650
61. Dufresne F, Stift M, Vergilino R, Mable BK. Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Molecular Ecology. 2014; 23: 40-69. doi: 10.1111/mec.12581 PMID: 24188632
62. Grattapaglia D, Sederoff R. Genetic Linkage Maps of Eucalyptus grandis and Eucalyptus urophylla Using a Pseudo-Testcross: Mapping Strategy and RAPD Markers. Genetics. 1994; 137: 1121-1137.PMID: 7982566
63. Garcia AAF, Kido EA, Meza NA, Souza HMB, Pinto LR, Pastina MM, Leite CS, da Silva JAG, Ulian EC, Figueira A, Souza AP. Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theor Appl Genet. 2006; 112: 298-314. PMID: 16307229
64. Gill BS, Friebe B, Endo TR. Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome. 1991; 34: 830-839.
65. Tuna M, Gill KS, Vogel KP. Karyotype and C-Banding Patterns of Mitotic Chromosomesin Diploid Bromegrass (Bromus riparius Rehm). Crop Sci. 2001; 41: 831-834.
66. Castiglioni P, Ajmone-Marsan P, van Wijk R, Motto M. AFLP markers in a molecular linkage map of maize: codominant scoring and linkage group distribution. Theor Appl Genet. 1999; 99: 425-431. doi: 10.1007/s001220051253 PMID: 22665174
67. Tanskley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Röder MS, Wing RA, Wu W, Young ND. High density molecular linkage maps of the tomato and potato genomes. Genetics. 1992; 132:1141-1160. PMID: 1360934
68. Okada M, Lanzatella C, Saha MC, Bouton J, Wu R, Tobias CM. Complete switchgrass genetic maps reveal subgenome collinearity, preferential pairing and multilocus interactions. Genetics. 2010; 185:745-760. doi: 10.1534/genetics.110.113910 PMID: 20407132
69. Pastina MM, Malosetti M, Gazaffi R, Mollinari M, Margarido GR, Oliveira KM, Pinto LR, Souza AP, van Eeuwijk FA, Garcia AAF. A mixed model QTL analysis for sugarcane multiple-harvest-location trial data. Theor. Appl. Genet. 2012; 124: 835-849. doi: 10.1007/s00122-011-1748-8 PMID: 22159754
70. Mendes-Bonato AB, Filho RGJ, Pagliarini MS, Valle CB, Penteado MIO. Unusual cytological patterns of microsporogenesis in Brachiaria decumbens: abnormalities in spindle and defective cytokinesis causing precocious cellularization. Cell Biol Int. 2002; 26: 641-646. PMID: 12127944
71. Tate JA, Soltis DE, Soltis PS. Polyploidy in Plants. In: Gregory TR (Ed.) The Evolution of the Genome. Elsevier, 2005. p. 371-426.
72. Stebbins GL. (1950) Variation and Evolution in Plants. New York: Columbia University Press.
73. Barcaccia G, Meneghetti S, Lucchin M, de Jong H. Genetic Segregation and Genomic Hybridization Patterns Support an Allopolyploid Structure and Disomic Inheritance for Salix Species. Diversity. 2014; 6: 633-651.
74. Risso-Pascotto C, Pagliarini MS, Valle CB. A new basic chromosome number for the genus Brachiaria (Trin.) Griseb. (Poaceae: Panicoideae: Paniceae). Genet Res Crop Evol. 2006; 53: 7-10.
75. Hojsgaard D, Horandl E. A little bit of sex matters for genome evolution in asexual plants. Frontiers in Plant Science. 2015; 6: 82. doi: 10.3389/fpls.2015.00082 PMID: 25750646
76. Mendes-Bonato AB, Pagliarini MS, Risso-Pascotto C, Valle CB. Chromosome number and meiotic behavior in Brachiaria jubata (Gramineae). J Genet. 2006; 85: 83-88. PMID: 16809846
77. Utsunomiya KS, Pagliarini MS, Valle CB. Microsporogenesis in tetraploid accessions of Brachiaria nigropedata (Ficalho & Hiern) Stapf (Gramineae). Biocell. 2005; 29: 295-301. PMID: 16524251
78. Pagliarini MS, Risso-Pascotto C, Souza-Kaneshima AM, Valle CB. Analysis of meiotic behavior in selecting potential genitors among diploid and artificially induced tetraploid accessions of Brachiaria ruziziensis (Poaceae). Euphytica. 2008; 164: 181-187.
79. Pikaard CS. Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol Biol. 2000; 43: 163-177. PMID: 10999402
80. Lewis MS Cheverud JM, Pikaard CS. Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana intercotype hybrids. Genetics. 2004; 167: 931-939. PMID: 15238541
81. Lewis MS, Pikaard DJ, Nasrallah M, Doelling JD, Pikaard CS. Locus-Specific ribosomal RNA gene silencing in nucleolar dominance. PLOS ONE. 2007; 8: 1-8.
82. Mendes-Bonato AB, Pagliarini MS, Valle Cb. Abnormal spindle orientation during microsporogenesis in an interspecific Brachiaria (Gramineae) hybrid. Genet. Mol Biol. 2006; 29: 122-125.
83. Santos JCS, Barreto MA, Oliveira FA, Vigna BBZ, Souza AP. Microsatellite markers for Urochloa humidicola (Poaceae) and their transferability to other Urochloa species. BMC Research Notes. 2015; 8:83 doi: 10.1186/s13104-015-1044-9 PMID: 25889143
84. Bitencourt GA, Chiari L, Valle CB, Salgado LR, Leguizamon GOC. Uso de marcadores RAPD na identificação de híbridos de Brachiaria humidicola. Boletim de Pesquisa, 23. Campo Grande: Embrapa Gado de Corte, 2008. 19p
85. Young BA, Sherwood RT, Bashaw EC. Cleared-pistyl and thick-sectioning techniques for detecting aposporous apomixis in grasses. Can J of Bot. 1979; 57: 1668-1672.
86. Vigna BBZ, Alleoni GC, Jungmann L, Valle CB, Souza AP. New microsatellite markers developed from Urochloa humidicola (Poaceae) and cross amplification in different Urochloa species. BMC Research Notes. 2011; 4:5-23.
87. Creste S, Tulmann Neto A, Figueira A. Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Molecular Biology Reporter. 2001; 19: 299-306.
88. Wu R, Ma CX, Painter I, Zeng ZB. Simultaneous maximum likelihood estimation of linkage and linkage phases in outcrossing species. Theor Pop Biol. 2002; 61: 349-363.
89. Margarido GRA, Souza AP, Garcia AAF. OneMap: software for genetic mapping in outcrossing species. Hereditas. 2007; 144: 78-79. PMID: 17663699
90. Wu R, Ma CX, Wu SS, Zeng ZB. Linkage mapping of sex-specific differences. Genetical Research. 2002; 79: 85-96. PMID: 11974606
91. Kosambi DD. The estimation of map distance from recombination values. Ann. Eug. 1944; 12: 172-175.