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Inheritance of leaf color in papaya

Abstract

Physiological disturbances are one of the major bottlenecks to the expansion of papaya crops due to the negative influence on fruit quality. Studies on genotypes of light-green color have become essential to the development of strategies of tolerance to the physiological disorder skin freckle. Understanding the inheritance of qualitative traits is crucial to selection and prediction of the behavior of segregating generations. Thus, this study aimed to determine the inheritance of the qualitative trait leaf color in segregating generations of crosses between the dark-green cultivar BSA and the light-green cultivar GPC. Inheritance was determined based on the Mendelian genetics laws, by evaluating the phenotypic proportions in the analysis of generations P1 (BSA), P2 (GPC), F1, F2, BC1, BC2, BC2r, and F2:3. The inheritance of light-green leaves from the crossing between BSA and GPG is due to double recessive epistasis.

Keywords:
Carica papaya L.; plant breeding; genetic variability; genetic control.

INTRODUCTION

Papaya (Carica papaya L.) is native to Central America or, more precisely, southern Mexico and Costa Rica (Chen et al. 1991Chen MH, Chen CC, Wang DN and Chen FC (1991) Somatic embryogenesis and plant regeneration from immature embryos of Carica papaya x Carica cauliflora cultured in vitro. Canadian Journal of Botany 69: 1913-1918. ). It is one of the most important tropical fruits worldwide and finds in Brazil favorable climatic conditions for its commercial exploitation. Therefore, the country has become one of the leading countries in papaya production (FAOSTAT 2016FAOSTAT - Food and Agriculture Organization of the United Nations Database (2016) Crops. Available at: < Available at: http://www.fao.org/faostat/en/#data/QC >. Acessed on October 11, 2018.
http://www.fao.org/faostat/en/#data/QC...
).

The search for new promising genotypes is crucial for the improvement of the crop. Initially, the knowledge about the genetic diversity directs the exploitation of the existing variability to be used in papaya breeding, aiming at new cultivars with different genotypic compositions (Silva et al. 2017Silva CA, Nascimento AL, Ferreira JP, Schmildt O, Malikouski RG, Alexandre RS, Ferreguetti GA and Schmildt ER (2017) Genetic diversity among papaya accessions. African Journal of Agricultural Research 12: 2041-2048. , Pereira et al. 2019Pereira MG, Luz LN, Santa-Catarina R, Ramos HCC, Pereira TNS, Barros GB, Ferregueti GA, Vivas MV, Cortes DFM, Vettorazzi JCF, Azecedo AON, Silveira SF, Oliveira JG and Viana AP (2019) UC10: a new early Formosa papaya cultivar. Crop Breeding and Applied Bietechnology 19: 131-134 ).

The diversity among accessions from germplasm banks, such as that of Caliman Agricola SA in Linhares - ES, has been reported by other authors (Barbosa et al. 2011 Barbosa CD, Viana AP, Quinta SSR and Pereira MG (2011) Artificial neural network analysis of genetic diversity in Carica papaya L. Crop Breeding and Applied Biotechnology 11: 224-231., Quintal et al. 2012Quintal SSR, Viana AP, Gonçalves LSA, Pereira MG and Júnior Amaral AT (2012) Divergência genética entre acessos de mamoeiro por meio de variáveis morfoagronômicas. Semina: Ciência Agrárias 33: 131-142. ). Also, contrasting phenotypes for the qualitative trait leaf color have been confirmed by different chlorophyll contents, including BSA, of dark-green color, and GPC, of light-green color (Silva et al. 2017Silva CA, Nascimento AL, Ferreira JP, Schmildt O, Malikouski RG, Alexandre RS, Ferreguetti GA and Schmildt ER (2017) Genetic diversity among papaya accessions. African Journal of Agricultural Research 12: 2041-2048. ).

Studies on generations analysis are scarce, and few qualitative traits of papaya regarding genetic control have been investigated (Costa et al. 2013aCosta AFS, Dantas JLL, Pereira MG, Cattaneo LF and Moreira SO (2013a) Cultura do mamoeiro: botânica, melhoramento e variedades. Informe Agropecuário 34: 14-24.). Qualitative traits usually have oligogenic inheritance, that is, they are controlled by few genes and are little influenced by the environment, which allows them to be exploited in a breeding program using hybridization. The expression of traits governed by few genes of greater effect have been shown to be important for breeding programs of several crops, mainly for those that work on the resistance response of plants to some diseases (Junghans et al. 2003Junghans DT, Alfenas AC, Brommonshenkel SH, Oda S, Mello EJ and Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter) in Eucalyptus mode of inheritance and mapping of a major gene with RAPD markers. Theoretical and Applied Genetics 108: 175-180. , Vijayalakshmi et al. 2005Vijayalakshmi S, Yadav K, Kushwaha C, Sarode SB, Srivastava CP, Chand R and Singh BD (2005) Identification of RAPD markers linked to the rust (Uromyces fabae) resistance gene in pea (Pisum sativum). Euphytica 144: 265-274., Batista et al. 2017Batista RO, Silva LC, Moura LM, Souza MH, Carneiro PCS, Sandes Carvalho Filho JLS and Carneiro JES (2017) Inheritance of resistance to fusarium wilt in common bean. Euphytica 213: 133., Costa et al. 2018Costa KDS, Santos AMM, Santos PR, Nascimento MR, Silva AMF, Albuquerque GMR, Batista RO, Pereira JWL and Carvalho Filho JLS (2018) Inheritance of resistance to Ralstonia pseudosolanacearum in tomato. Euphytica 213: 133.).

Studies aiming at obtaining genotypes with light-green color have been carried out for these genotypes have tolerance to the physiological disorder known as skin freckle (Oliveira and Vitoria 2011Oliveira JG and Vitoria AP (2011) Papaya: nutritional and pharmacological characterization, and quality loss due to physiological disorders. An overview. Food Research International 44: 1306-1313. , Pinto et al. 2013aPinto FO, Pereira MG, Luz LN, Cardoso DL, Ramos HCC and Macedo CMP (2013a) Use of microsatellite markers in molecular analysis of segregating populations of papaya (Carica papaya L.) derived from backcrossing. Genetics and Molecular Research 12: 2248-2259. , Pinto et al. 2013bPinto FO, Ramos HCC, Cardoso DL, Luz LN and Pereira MG (2013b) Development of papaya genotypes (Carica papayaL.) tolerant to skin freckles. Revista Brasileira de Fruticultura 35: 1101-1115. ). Skin freckle has caused significant losses to the export market of papaya, which is much more demanding when it comes to the external appearance of the fruits. Therefore, this trait has become relevant for a crop breeding program and has been studied by several authors (Kaiser et al. 1996Kaiser C, Allan P, White BJ and Dehrmann FM (1996) Some morphological aspects of freckle on papaya (Carica papaya L.) fruit. Journal of South African Society Horticulturae 6: 37-40., Campostrini et al. 2005Campostrini E, Lima HC, Oliveira JG, Monnerart PH and Marinho CS (2005) Teores de Ca e variáveis meteorológicas: relações com a mancha fisiológica do mamão no norte fluminense. Bragantia 64: 601-613. , Gomes Filho et al. 2006Gomes Filho A, Oliveira JG, Viana AP, Damasceno Júnior PC and Pereira MG (2006) Validação do método das notas para quantificação da incidência da mancha fisiológica do mamão através do uso de imagens digitais. Revista Brasileira de Fruticultura 28: 365-368. , Gomes Filho et al. 2007Gomes Filho A, Oliveira JG, Viana AP, Damasceno Júnior PC and Pereira MG (2007) Lâminas de irrigação e coberturas do solo sobre a incidência da mancha fisiológica e produtividade do mamão ‘Golden’. Ciência Rural 37: 1654-1660. ).

In a study with five papaya genotypes, Torres Netto et al. (2009Torres Netto A, Campostrini E, Azevedo LC, Souza MA, Ramalho JC and Chaves MM (2009) Morphological analysis and photosynthetic performance of improved papaya genotypes. Brazilian Journal Plant of Physiology 21: 209-222. ) highlighted that cv. Golden, for its light-green color, was the only one without midday depression of photosynthesis. They also reported that this property is the most relevant since the high temperature and high light incidence are common in the main areas of papaya production in Brazil. Torres Netto et al. (2009Torres Netto A, Campostrini E, Azevedo LC, Souza MA, Ramalho JC and Chaves MM (2009) Morphological analysis and photosynthetic performance of improved papaya genotypes. Brazilian Journal Plant of Physiology 21: 209-222. ) state that further papaya breeding programs should be planned to incorporate some qualitative traits from light-green leaves genotypes.

Understanding the inheritance of leaf color is crucial to breeding programs as it supports the release of new cultivars and favors research strategies to avoid wasting time with inefficient breeding methods. The knowledge of the nature and magnitude of the gene effects that control a given trait is fundamental for the selection and prediction of the behavior of segregating and hybrid generations (Cruz et al. 2012Cruz CD, Regazzi AJ and Carneiro PCS (2012) Modelos biométricos aplicados ao melhoramento genético. UFV, Viçosa, 514p.). Thus, this work aimed to analyze the inheritance of the qualitative trait leaf color in papaya.

MATERIAL AND METHODS

The study of the oligogenic inheritance requires some steps to be followed. The contrasting parents selected for the trait leaf color were the lines BSA, of dark-green leaves, and GPC, of light-green leaves. Seeds of BSA and GPC genotypes were obtained from potentially inbred populations, maintained for more than eight self-fertilization generations in the germplasm bank of Caliman Agrícola S.A. Both parents had their morpho-agronomic traits described by Silva et al. (2017Silva CA, Nascimento AL, Ferreira JP, Schmildt O, Malikouski RG, Alexandre RS, Ferreguetti GA and Schmildt ER (2017) Genetic diversity among papaya accessions. African Journal of Agricultural Research 12: 2041-2048. ).

The experiment was carried out at Santa Teresinha Farm, belonging to Caliman Agrícola SA, in the municipality of Linhares, Espírito Santo (lat 19° 11' 49" S, long 40° 05' 52" W, alt 30 m asl), between February 2012 and December 2014 (Figure 1). The climate of the region is classified as type AWi (tropical humid), with rainy summer and dry winter (Alvares et al. 2013Alvares CA, Stape, JL, Sentelhas PC, Gonçalves JLM and Sparovek G (2013) Koppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.).

Figure 1
Planting schedule and seed collection of the study generations from the cross P1 (BSA) x P2 (GPC).

The inheritance of leaf color in papaya was studied by the analysis of the generations P1 (BSA), P2 (GPC), F1, F2=, BC1, BC2, BC2r (BC2 reciprocal), and F2:3. The first planting of the parents was carried out in February 2012, and eight months later, GPC was used as a pollen donor to BSA to produce the F1 population. Afterward, seeds were sown in November 2012, together with the parents, to produce populations F2, BC1, BC2, and BC2r, and to maintain P1, P2, and F1 seeds in 2013.

The F1 generation was self-fertilized to produce the F2generation. Backcrossings were performed as follows: BC1 was obtained by crossing BSA, as the female parent, and F1, as the male parent; BC2 was obtained by crossing GPC, as the female parent, and F1, as the male parent; and BC2r was obtained by crossing F1, as the female parent, and GPC, as the male parent. The reciprocal cross was carried out to examine possible maternal control for the studied trait.

Seeds of all generations were planted in the field in November 2013. All hermaphroditic plants were evaluated: 16 from parent P1; 16 from parent P2; 23 from the F1 generation, to evaluate the environmental effect; 168 from the F2 generation; 41 from BC1; 55 from BC2; and 54 from BC2r.

In the F2 generation, seven plants of different colors were selected: dark-green leaves (5, 7, 8, and 9) and light-green leaves (1, 2, and 4) leaves. These plants were crossed and self-fertilized to obtain the F2:3 generation (F3 generation derived from the F2 generation selected). The self-fertilized plants 1, 5, 7, and 9 and the three 2x1, 2x4, and 8x7 crosses were planted in the field in May 2015. Hermaphroditic plants from each treatment of the F2:3 generation (15, 27, 26, 36, 31, 32, and 26 hermaphroditic plants) were evaluated to confirm the phenotypic segregation and the genetic control of the trait, based on the Mendelian laws.

Manual pollination was performed by transferring the pollen from a hermaphroditic plant to the stigma of a female plant. Hermaphroditic plants that did natural pollination were used for the self-fertilization. All procedures were performed before anthesis, preventing the pollination from other plants. Flowers were marked and protected with paper bags. All populations were obtained in the field.

The experiment was carried out with one hermaphroditic plant per hole, which were spaced at 3.6 m between rows and 1.5 m within rows, following cultural practices recommended for the crop (Costa et al. 2013bCosta NA, Costa AFS and Ferreguetti GA (2013b) Manejo da fertilidade do solo e da nutrição do mamoeiro. Informe Agropecuário 34: 38-47.).

The analysis of the inheritance of the qualitative trait was based on the Mendelian laws, where the phenotypic proportions in F2, backcross, and subsequent generations were evaluated. This procedure was carried out for leaf color in the segregating generations and was divided into two classes (dark-green and light-green), the same pattern shown by the parents BSA (dark-green) and GPC (light-green).

Plant phenotypes were analyzed at 300 days after planting when the plants were clearly distinguished between dark-green and light-green leaves. The description of each phenotype was confirmed by the chlorophyll content index (CCI), quantified with a portable chlorophyll meter ClorofiLOG® CFL 1030, according to the manufacturer's instructions (Falker 2008Falker Automação Agrícola Ltda (2008) Manual do medidor eletrônico de teor clorofila (ClorofiLOG/CFL 1030). Falker Automação Agrícola, Porto Alegre, 10p.), and the frequency distribution for BSA and GPC was graphically displayed. The leaf color variability in papaya was confirmed by the CCI and analyzed for the physiological traits, based on Castro et al. (2011Castro FA, Campostrini E, Torres Netto A and Viana LH (2011) Relationship between photochemical efficiency (JIP-Test Parameters) and portable chlorophyll meter readings in papaya plants. Brazilian Journal of Plant Physiology 23: 295-304. ), who observed that the light-green color of the papaya leaves could be confirmed by the lower CCI values.

The analysis of the color, with a discrete distribution, was carried out by the genetic hypothesis test. This test allows determining the predominant segregation pattern that indicates whether it is governed by one, two, or more genes, as well as the predominant type of interaction (Liu 1997Liu BH (1997) Statistical genomics: linkage mapping and QTL analysis. CRC Press, Boca Raton, 119p.). The chi-square test has been proven to be practical and efficient in testing the hypotheses of segregation patterns (Batista et al. 2017Batista RO, Silva LC, Moura LM, Souza MH, Carneiro PCS, Sandes Carvalho Filho JLS and Carneiro JES (2017) Inheritance of resistance to fusarium wilt in common bean. Euphytica 213: 133.) for it considers the deviations between expected and observed values ​​and the number evaluated (Schuster and Cruz 2004Schuster I and Cruz CD (2004) Estatística genômica aplicada a população derivadas de cruzamentos. Editora UFV, Viçosa , 568p.).

The chi-square test (X 2) used to verify the ratio of segregation in all populations with its particularities is given by:

χ 2 = i = 1 n O b s i - E x p i 2 E x p i

where:

X2is the calculated chi-square value;

Obsi and Exp i are the observed and expected values ​​for the ith phenotypic class (i = 1, 2, ... n), respectively.

Analyses were performed for non-parametric chi-square test at 5% of probability, using the Genes software (Cruz 2016Cruz CD (2016) Genes Software - extended and integrated with the R, Matlab and Selegen. Acta Scientiarum. Agronomy 38: 547-552.).

RESULTS AND DISCUSSION

Table 1 shows the phenotypic frequencies based on the leaf color (dark-green or light-green). The BSA parent (dark-green leaf) had a mean CCI of 58.50 ± 2.32, while the GPC parent (light-green color), had CCI of 47.19 ± 2.86. The CCI is a continuous random variable, and its frequency distribution is shown in Figure 2, where the light- and dark-green colors form very distinct classes. A normal distribution is observed for the CCI data (BSA with p-value = 0.7733 and GPC p-value = 0.6994 by the Shapiro-Wilk test). All the plants in the F1 generation had dark-green leaves, indicating that the light-green color is controlled by recessive gene(s).

Table 1
Summary of frequencies observed, chi-square test, and genotypes for the seven generations in the study of leaf color in papaya in the analysis of generations, with plants evaluated at 300 days after planting

Figure 2
Frequency distribution of CCI values of papaya leaves of BSA and GPC genotypes.

Lee (1988Lee DW (1988) Simulating forest shade to study the development ecology of tropical plants: juvenile growth in three vines in India. Journal of Tropical Ecology 4: 281-292. ), in a study with grape, reported that the chlorophyll content varies greatly between species and between genotypes of the same species. This variability was also found in papaya and is likely to be explored in breeding programs, and its physiological aspect has been studied by several authors (Torres Netto et al. 2002Torres Netto A, Campostrini E, Oliveira JG and Yamanishi OK (2002) Portable chlorophyll meter for the quantification of photosynthetic pigments, nitrogen and the possible use for assessment of the photochemical process in Carica papaya L. Brazilian Journal of Plant Physiology 14: 203-210. , Castro et al. 2011Castro FA, Campostrini E, Torres Netto A and Viana LH (2011) Relationship between photochemical efficiency (JIP-Test Parameters) and portable chlorophyll meter readings in papaya plants. Brazilian Journal of Plant Physiology 23: 295-304. ).

Castro et al. (2014Castro FA, Campostrini E, Netto AT, Menezes AG, Ferraz TM and Glenn DM (2014) Portable chlorophyll meter (PCM-502) values are related to total chlorophyll concentration and photosynthetic capacity in papaya (Carica papaya L.). Theoretical Experimental Plant Physiology 26: 201-210. ) found that papaya genotypes with different leaf colors had CCIs ​​ related to total chlorophyll concentrations, quantified by a destructive method. The genotype with light-green leaf partitioned less nitrogen for chlorophyll synthesis when compared with the genotype with dark-green leaf. Moreover, the latter was more sensitive to PSII (photosystem II) damage when nitrogen was scarce.

In the F2 generation, the segregation for the color trait was 9 dark-green: 7 light-green (X 2=0.732, p-value=0.3923) indicating digenic inheritance with double recessive epistasis (Phillips 2008Phillips PC (2008) Epistasis - the essential role of gene interactions in the structure and evolution of genetic systems. Nature Review Genetics 9: 855-867. , Griffiths et al. 2015Griffiths AJF, Wessler SR, Carroll SB and Doebley J (2015) Introduction to genetic analysis. 11th edn, W. H. Freeman, New York, 58p.). This result shows that the dark-green color is controlled by at least one dominant allele, simultaneously in the two loci. The light-green color includes genotypes with a dominant allele in only one of the loci and the genotype with double recessive alleles. The inheritance hypothesis that the characteristic leaf color is controlled by a gene that segregates 3 dark- green: 1 light-green in F2 and the hypothesis that it is controlled by three genes that segregate 27 dark-green: 37 light-green in F2 were also tested. The segregation shown in this study did not fit into any of these hypotheses by the chi-square test (Table 1).

The genotypes in each generation are represented in Table 1, where the dark-green color shows at least one dominant allele for each locus (AABB; AaBb; AABb; AaBB) and the light-green color shows at least one locus with all recessive alleles (AAbb; Aabb; aaBB; aaBb; aabb).

The dark-green color of all plants in BC1 indicates that the genotypes of this generation have at least one dominant allele in each locus. When adjusting to the proportion of 1 dark-green: 3 light-green in BC2 (X 2=0.006, p-value=0.9379), the dark-green color is represented by the genotype with both loci in heterozygosity, while the color of the light-green plants is controlled by a locus with both recessive alleles. The BC2r generation had plants at the proportion of 1 dark-green: 3 light-green, indicating the absence of maternal effects in the expression of the leaf color.

Cassetari et al. (2015Cassetari LS, Gomes MS, Santos DC, Santiago WD, Andrade J, Guimaraes AC, Souza JÁ, Cardoso MG, Maluf WR and Gomes LA (2015) β-Carotene and chlorophyll levels in cultivars and breeding lines of lettuce. Acta Horticulturae 1083: 469-474. ) studied lettuce and reported different shades of green and a relative number of deleterious mutants. These mutants were genetically identified, and all of them indicated that the reduction in the green color (chlorophyll) corresponds to recessive alleles.

The phenotypic frequencies of the F2:3 are shown in Table 2. Four plants selected in the F2 (1, 5, 7, and 9) were self-fertilized. In the self-fertilization of plant 1 (light-green phenotype), all progenies had light-green color (45.74 ± 2.41 CCI) since they showed at least one locus in recessive homozygosity. Conversely, in the self-fertilization of plant 9 (dark-green phenotype), all progenies had dark-green color (58.97 ± 3.83 CCI), indicating that their plant has all dominant alleles.

Table 2
Summary of frequencies observed, chi-square test, and genotypes at generation F2:3, for the seven genotypes and crosses selected in F2 in the study of leaf color in papaya, at 300 days after planting

The dark-green plants 5 and 7 had progenies with segregation of 3 dark-green: 1 light-green (60.28 ± 2.59 and 45.57 ± 2.45; 60.84 ± 3.64; and 45.88 ± 2.55 CCI) (X 2=0.111, p-value=0.7389; X 2=0.461, p-value=0.4669) (Table 2), indicating that plants 5 and 7 have one locus with all dominant alleles and the other locus with one dominant allele and one recessive allele. Figure 3 shows the dark-green and light-green leaves progenies from plant 5.

Figure 3
Difference in leaf color of papaya originated from self-fertilization of plant 5 at seven months after planting; in the foreground, dark-green plant to the left and light-green plant to the right.

Plants 1, 2, and 4 (light-green color) and 8 and 7 (dark-green color) generated crosses (2x1, 2x4 and 8x7). For 2x1 and 2x4, all light-green progenies were obtained, showing mean CCI values of 46.69 ± 2.83 and 46.34 ± 2.80, respectively. This result indicates that all the parents have the same locus with two recessive alleles (AAbb or aaBB) and that when crossing all their progenies, the latter has a locus in recessive homozygosity, which controls the light-green color. However, the cross between light-green parents with different loci with recessive alleles (AAbb x aaBB) would produce all progenies with dark-green color, and therefore, after the selection of the light-green color genotype, self-fertilization favors the fixation of this trait. The segregation in the cross 8x7 was 3 dark-green: 1 light-green (62.15 ± 2.75 and 44.56 ± 1.00 CCI) (X 2=0.605, p-value=0.4669), showing that the two plants have the same locus with dominant alleles and a heterozygous locus.

The lowest means for the CCI variable were found for the genotypes with light-green leaf of the cross 8x7 (44.56 ± 1.00). All means were ​​higher than 40, which is associated with high photosynthetic pigment values ​​(chlorophylls a and b and carotenoids) and nitrogen content in papaya leaves (Torres Netto et al. 2002Torres Netto A, Campostrini E, Oliveira JG and Yamanishi OK (2002) Portable chlorophyll meter for the quantification of photosynthetic pigments, nitrogen and the possible use for assessment of the photochemical process in Carica papaya L. Brazilian Journal of Plant Physiology 14: 203-210. ).

Knowing the digenic inheritance with dual recessive epistasis, from crosses between BSA and GPC, the possibility of incorporating the light-green color into new commercial cultivars becomes an interesting prospect for the papaya breeding.

ACKNOWLEDGMENTS

The authors thank CNPq, CAPES, and FAPES, for the scholarship granted, and Caliman Agrícola S.A., for the technical support.

REFERENCES

  • Alvares CA, Stape, JL, Sentelhas PC, Gonçalves JLM and Sparovek G (2013) Koppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.
  • Barbosa CD, Viana AP, Quinta SSR and Pereira MG (2011) Artificial neural network analysis of genetic diversity in Carica papaya L. Crop Breeding and Applied Biotechnology 11: 224-231.
  • Batista RO, Silva LC, Moura LM, Souza MH, Carneiro PCS, Sandes Carvalho Filho JLS and Carneiro JES (2017) Inheritance of resistance to fusarium wilt in common bean. Euphytica 213: 133.
  • Campostrini E, Lima HC, Oliveira JG, Monnerart PH and Marinho CS (2005) Teores de Ca e variáveis meteorológicas: relações com a mancha fisiológica do mamão no norte fluminense. Bragantia 64: 601-613.
  • Cassetari LS, Gomes MS, Santos DC, Santiago WD, Andrade J, Guimaraes AC, Souza JÁ, Cardoso MG, Maluf WR and Gomes LA (2015) β-Carotene and chlorophyll levels in cultivars and breeding lines of lettuce. Acta Horticulturae 1083: 469-474.
  • Castro FA, Campostrini E, Torres Netto A and Viana LH (2011) Relationship between photochemical efficiency (JIP-Test Parameters) and portable chlorophyll meter readings in papaya plants. Brazilian Journal of Plant Physiology 23: 295-304.
  • Castro FA, Campostrini E, Netto AT, Menezes AG, Ferraz TM and Glenn DM (2014) Portable chlorophyll meter (PCM-502) values are related to total chlorophyll concentration and photosynthetic capacity in papaya (Carica papaya L.). Theoretical Experimental Plant Physiology 26: 201-210.
  • Chen MH, Chen CC, Wang DN and Chen FC (1991) Somatic embryogenesis and plant regeneration from immature embryos of Carica papaya x Carica cauliflora cultured in vitro Canadian Journal of Botany 69: 1913-1918.
  • Costa AFS, Dantas JLL, Pereira MG, Cattaneo LF and Moreira SO (2013a) Cultura do mamoeiro: botânica, melhoramento e variedades. Informe Agropecuário 34: 14-24.
  • Costa NA, Costa AFS and Ferreguetti GA (2013b) Manejo da fertilidade do solo e da nutrição do mamoeiro. Informe Agropecuário 34: 38-47.
  • Costa KDS, Santos AMM, Santos PR, Nascimento MR, Silva AMF, Albuquerque GMR, Batista RO, Pereira JWL and Carvalho Filho JLS (2018) Inheritance of resistance to Ralstonia pseudosolanacearum in tomato. Euphytica 213: 133.
  • Cruz CD, Regazzi AJ and Carneiro PCS (2012) Modelos biométricos aplicados ao melhoramento genético. UFV, Viçosa, 514p.
  • Cruz CD (2016) Genes Software - extended and integrated with the R, Matlab and Selegen. Acta Scientiarum. Agronomy 38: 547-552.
  • Falker Automação Agrícola Ltda (2008) Manual do medidor eletrônico de teor clorofila (ClorofiLOG/CFL 1030). Falker Automação Agrícola, Porto Alegre, 10p.
  • FAOSTAT - Food and Agriculture Organization of the United Nations Database (2016) Crops. Available at: < Available at: http://www.fao.org/faostat/en/#data/QC >. Acessed on October 11, 2018.
    » http://www.fao.org/faostat/en/#data/QC
  • Gomes Filho A, Oliveira JG, Viana AP, Damasceno Júnior PC and Pereira MG (2006) Validação do método das notas para quantificação da incidência da mancha fisiológica do mamão através do uso de imagens digitais. Revista Brasileira de Fruticultura 28: 365-368.
  • Gomes Filho A, Oliveira JG, Viana AP, Damasceno Júnior PC and Pereira MG (2007) Lâminas de irrigação e coberturas do solo sobre a incidência da mancha fisiológica e produtividade do mamão ‘Golden’. Ciência Rural 37: 1654-1660.
  • Griffiths AJF, Wessler SR, Carroll SB and Doebley J (2015) Introduction to genetic analysis. 11th edn, W. H. Freeman, New York, 58p.
  • Junghans DT, Alfenas AC, Brommonshenkel SH, Oda S, Mello EJ and Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter) in Eucalyptus mode of inheritance and mapping of a major gene with RAPD markers. Theoretical and Applied Genetics 108: 175-180.
  • Kaiser C, Allan P, White BJ and Dehrmann FM (1996) Some morphological aspects of freckle on papaya (Carica papaya L.) fruit. Journal of South African Society Horticulturae 6: 37-40.
  • Lee DW (1988) Simulating forest shade to study the development ecology of tropical plants: juvenile growth in three vines in India. Journal of Tropical Ecology 4: 281-292.
  • Liu BH (1997) Statistical genomics: linkage mapping and QTL analysis. CRC Press, Boca Raton, 119p.
  • Oliveira JG and Vitoria AP (2011) Papaya: nutritional and pharmacological characterization, and quality loss due to physiological disorders. An overview. Food Research International 44: 1306-1313.
  • Pereira MG, Luz LN, Santa-Catarina R, Ramos HCC, Pereira TNS, Barros GB, Ferregueti GA, Vivas MV, Cortes DFM, Vettorazzi JCF, Azecedo AON, Silveira SF, Oliveira JG and Viana AP (2019) UC10: a new early Formosa papaya cultivar. Crop Breeding and Applied Bietechnology 19: 131-134
  • Phillips PC (2008) Epistasis - the essential role of gene interactions in the structure and evolution of genetic systems. Nature Review Genetics 9: 855-867.
  • Pinto FO, Pereira MG, Luz LN, Cardoso DL, Ramos HCC and Macedo CMP (2013a) Use of microsatellite markers in molecular analysis of segregating populations of papaya (Carica papaya L.) derived from backcrossing. Genetics and Molecular Research 12: 2248-2259.
  • Pinto FO, Ramos HCC, Cardoso DL, Luz LN and Pereira MG (2013b) Development of papaya genotypes (Carica papayaL.) tolerant to skin freckles. Revista Brasileira de Fruticultura 35: 1101-1115.
  • Quintal SSR, Viana AP, Gonçalves LSA, Pereira MG and Júnior Amaral AT (2012) Divergência genética entre acessos de mamoeiro por meio de variáveis morfoagronômicas. Semina: Ciência Agrárias 33: 131-142.
  • Schuster I and Cruz CD (2004) Estatística genômica aplicada a população derivadas de cruzamentos. Editora UFV, Viçosa , 568p.
  • Silva CA, Nascimento AL, Ferreira JP, Schmildt O, Malikouski RG, Alexandre RS, Ferreguetti GA and Schmildt ER (2017) Genetic diversity among papaya accessions. African Journal of Agricultural Research 12: 2041-2048.
  • Torres Netto A, Campostrini E, Azevedo LC, Souza MA, Ramalho JC and Chaves MM (2009) Morphological analysis and photosynthetic performance of improved papaya genotypes. Brazilian Journal Plant of Physiology 21: 209-222.
  • Torres Netto A, Campostrini E, Oliveira JG and Yamanishi OK (2002) Portable chlorophyll meter for the quantification of photosynthetic pigments, nitrogen and the possible use for assessment of the photochemical process in Carica papaya L. Brazilian Journal of Plant Physiology 14: 203-210.
  • Vijayalakshmi S, Yadav K, Kushwaha C, Sarode SB, Srivastava CP, Chand R and Singh BD (2005) Identification of RAPD markers linked to the rust (Uromyces fabae) resistance gene in pea (Pisum sativum). Euphytica 144: 265-274.

Publication Dates

  • Publication in this collection
    01 Aug 2019
  • Date of issue
    Apr-Jul 2019

History

  • Received
    27 Nov 2017
  • Accepted
    14 Dec 2018
Crop Breeding and Applied Biotechnology Universidade Federal de Viçosa, Departamento de Fitotecnia, 36570-000 Viçosa - Minas Gerais/Brasil, Tel.: (55 31)3899-2611, Fax: (55 31)3899-2611 - Viçosa - MG - Brazil
E-mail: cbab@ufv.br