Abstract
Carica papaya is a trioecious species, which means its plants can exist in three sex forms, namely female (XX), male (XY), and hermaphrodite (XYh). Though infrequent, sex reversal from XY to XYh or vice versa may occur in these plants. This study proposes to investigate the genetic identity of a hermaphrodite plant (M3) identified in a dioecious progeny, determining whether sex reversal or contamination occurred. The following 16 genotypes belonging to the active germplasm bank of papaya of UENF/Caliman were analyzed: eight genotypes of the dioecious progeny (seven females and one male), one hermaphrodite genotype (M3) and seven controls (three females and four hermaphrodites). PCR was performed with 66 loci from the HSY and autosomal regions, in addition to three locus-specific primers. The genetic dissimilarity matrix obtained by the weighted index was used to cluster the individuals via the UPGMA hierarchical method and to project the distances onto the two-dimensional plane. Heterozygosity and inbreeding coefficients were estimated for each accessed region. In terms of descriptive parameters, genotype M3 was similar to the hermaphrodite controls in the HSY region and to the dioecious genotypes in the autosomal region. In the cluster analysis, genotype M3 was near the dioecious genotypes for the HSY region and near the hermaphrodites for the autosomal region. The analysis of distance projection onto the two-dimensional plane corroborated the clustering observed for the 30 loci together. Based on the analysis of the male-specific locus, the hypothesis of occurrence of natural sex reversal was discarded, indicating probable contamination.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AGP:
-
Active germplasm bank
- AFLP:
-
Amplified fragment length polymorphism
- HSY:
-
Hermaphrodite-specific region of the Yh chromosome
- MSY:
-
Male-specific region of the Y chromosome
- Ho:
-
Observed heterozygosity
- f :
-
Inbreeding coefficient
- PCoA:
-
Principal coordinate analysis
- PCR:
-
Polymerase chain reaction
- RAPD:
-
Random amplified polymorphic DNA
- SCAR:
-
Sequence characterized amplified region
- SSR:
-
Simple sequence repeats
- UPGMA:
-
Unweighted pair group method with arithmetic mean
References
Arkle Junior TD, Nakasone HY (1984) Floral differentiation in the hermaphroditic papaya. Hortic Sci 19:832–834
Aryal R, Ming R (2014) Sex determination in flowering plants: papaya as a model system. Plant Sci 217–218:56–62. https://doi.org/10.1016/j.plantsci.2013.10.018
Awada M (1958) Relationships of minimum temperature and growth rate with sex expression of papaya plants (Carica papaya L.). Hawaii Agric Exp Stn Tech Bull 38:1–16
Chaves-Bedoya G, Nunez VA (2007) Scar marker for the sex types determination in Colombian genotypes of Carica papaya. Euphytica 153:215–220. https://doi.org/10.1007/s10681-006-9256-7
Cruz CD (2013) GENES—a software package for analysis in experimental statistics and quantitative genetics. Acta Scientiarum 35:271–276. https://doi.org/10.4025/actasciagron.v35i3.21251
Daher RF et al (2002) Genetic divergence among elephantgrass cultivars assessed by rapd markers in composit samples. Scientia Agricola 59(4):623–627. https://doi.org/10.1590/S0103-90162002000400001
Damasceno Júnior PC et al (2008) Comportamento floral de híbridos de mamoeiro (Carica papaya L.) avaliados no verão e primavera. Ceres 55(4):310–316
Deputy JC et al (2002) Molecular markers for sex determination in papaya (Carica papaya L.). Theor Appl Genet 106(1):107–111. https://doi.org/10.1007/s00122-002-0995-0
Development Core Team (2011) R: a language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts offresh leaf tissue. Phytochem Bull 19:11–15
Eustice M et al (2008) Development and application of microsatellite markers for genomic analysis of papaya. Tree Genet Genomes 4:333–341. https://doi.org/10.1007/s11295-007-0112-2
Gomes Oliveira AM et al (1994) Mamão para exportação: aspectos técnicos da produção I. Ministério da Agricultura do Abastecimento e da Reforma Agrária. Secretaria de Desenvolvimento Rural. Programa de Apoio à Produção e Exportação de Frutas. Hortaliças. Flores e Plantas Ornamentais. Brasília: EMBRAPA-SPI. 52 p. (Série Publicações Técnicas FRUPEX; 9)
Hofmeyr JDJ (1939) Sex reversal in Carica papaya L. South Afr J Sci 36:286–287
Lemos EGM et al (2002) Identification of sex in Carica papaya L. using RAPD markers. Euphytica 127:179–184. https://doi.org/10.1023/A:1020269727772
Liao Z et al (2017) Development of male-specific markers and identification of sex reversal mutants in papaya. Euphytica 213:53. https://doi.org/10.1007/s10681-016-1806-z
Liu K, Muse SV (2005) Power Marker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Liu Z et al (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348–352. https://doi.org/10.1038/nature02228
Ma H et al (2004) High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 166(1):419–436. https://doi.org/10.1534/genetics.166.1.419
Na J-K et al (2012) Construction of physical maps for the sex-specific regions of papaya sex chromosomes. BMC Genom 13:176. https://doi.org/10.1186/1471-2164-13-176
Negrutiu I et al (2001) Dioecious plants. A key to the early events of sex chromosome evolution. Plant Physiol 127(4):1418–1424. https://doi.org/10.1104/pp.010711
Nunes GS, Ribeiro MC (1999) Pesticidas: uso, legislação e controle. Pesticidas: Revista de Ecotoxicologia e Meio Ambiente 9:31–34
Oliveira AMG et al (1994) Mamão para exportação: aspectos técnicos da produção. Brasília, DF: EMBRAPA-SPI, 52p. (FRUPEX. Série de publicações técnicas)
Oliveira EJ et al (2007) Marcadores moleculares na predição do sexo em plantas de mamoeiro. Pesq. agropec. bras. 42(12):1747–1754
Oliveira EJ et al (2010) Polymorphism microsatellite markers set for Carica papaya L. and its use in molecular-assisted selection. Euphytica 173:279–287. https://doi.org/10.1007/s10681-010-0150-y
Parasnis AS et al (1999) Microsatellite (GATA)n reveals sex specific differences in papaya. Theor Appl Genet 99:1047–1052. https://doi.org/10.1007/s001220051413
Parasnis AS et al (2000) A highly reliable sex diagnostic PCR assay for mass screening of papaya seedlings. Mol Breed 6:337–344. https://doi.org/10.1023/A:1009678807507
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Ramos HCC et al (2011) Comparison of multiallelic distances for the quantification of genetic diversity in the papaya. Acta Scientiarum Agron 33(1):59–66. https://doi.org/10.4025/actasciagron.v33i1.11698
Ramos HCC et al (2014) Genetic-molecular characterization of backcross generations for sexual conversion in papaya (Carica papaya L.). Genet Mol Res 13(4):10367–10381. https://doi.org/10.4238/2014
Santos SC et al (2003) A microsatellite library for Carica papaya L. cv Sunrise Solo. Revista Brasileira de Fruticultura 25:263–267. https://doi.org/10.1590/S0100-29452003000200020
Silva FF et al (2007a) DNA-Marker-assisted sex conversion in elite papaya genotype (Carica papaya L.). Breed Appl Biotechnol 7:52–58. https://doi.org/10.12702/1984-7033.v07n01a08
Silva FF et al (2007b) Evaluation of the sexual expression in a segregating BC1 papaya population. Crop Breed Appl Biotechnol 7:16–23. https://doi.org/10.12702/1984-7033.v07n01a03
Sondur SN et al (1996) A genetic linkage map of papaya based on randomly amplified polymorphic DNA markers. Theor Appl Genet 93:547–553. https://doi.org/10.1007/BF00417946
Storey WB (1953) Genetics of the papaya. J Hered 44(2):70–78. https://doi.org/10.1093/oxfordjournals.jhered.a106358
Storey WB (1958) Modifications of sex expression in Papaya. Adv Hortic 2:49–60
Urasaki N et al (2002) A male and hermaphrodite specific RAPD marker for papaya (Carica papaya L.). Theor Appl Genet 104:281–285. https://doi.org/10.1007/s001220100693
Van Buren R et al (2015) Origin and domestication of papaya Yh chromosome. Genome Res 25:524–533. https://doi.org/10.1101/gr.183905.114
Vivas M et al (2012) Patometria, parâmetros genéticos e reação de progênies de mamoeiro à pinta-preta. Bragantia 71:235–238. https://doi.org/10.1590/S0006-87052012005000021
Vivas M et al (2014) Seleção de progênies femininas de mamoeiro para resistência a mancha-de-phoma via modelos mistos. Bragantia 73(4):446–450. https://doi.org/10.1590/1678-4499.216
Vyskot B, Hobza R (2004) Gender in plants: sex chromosomes are emerging from the fog. Trends Genet 20(9):432–438. https://doi.org/10.1016/j.tig.2004.06.006
Wang J et al (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA 109:13710–13715. https://doi.org/10.1073/pnas.1207833109
Funding
“This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001”. We also thank the Carlos Chagas Filho Foundation for Research Support of the State of Rio de Janeiro (FAPERJ) and the National Council for Scientific and Technological Development (CNPq) for granting scholarships and project financing and the Company Caliman Agrícola S/A (CALIMAN) for logistical support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pirovani, A.A.V., Ramos, H.C.C., Santa-Catarina, R. et al. A hermaphrodite genotype in dioecious papaya progeny: sex reversal or contamination?. Euphytica 214, 227 (2018). https://doi.org/10.1007/s10681-018-2304-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-018-2304-2