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Heterotic potential for Physalis peruviana fruit traits in hybrid combinations

Potencial Heterótico de Combinações Híbridas de Physalis peruviana para Caracteres de Fruto

Abstract:

The breeding of Physalis peruviana is incipient in Brazil and is shown to be the most promising alternative for the development of productive genotypes with fruit quality. Therefore, the objective was to evaluate the combining ability between inbred lines of P. peruviana, thus indicating the selection of hybrids with fruit quality. Therefore, four populations from different origins were selfed for three generations and crossed in controlled hybridizations, resulting in 28 P. peruviana populations. The hybrid in relation to the parent performance, based on the effects of general and specific combining ability, was compared in a full diallel mating design (Griffing Method 1). In the analysis of variance, the factor genotype was partitioned into the following causes of variation: i) parents and F1 hybrids, ii) selfed generations and iii) Genotype × environment (GE) interaction. There were significant differences between Parents and F1 hybrids for the trait fruit polar diameter. Still, the interaction between specific combining ability x environment and, reciprocal effect x environment, was significant. However, for the Xanxerê environment, there was a reduction of approximately 3.0 mm in the polar diameter of the fruit in the hybrid Colombia x Peru and a reduction of 4.5 mm for the reciprocal (Peru x Colombia). In the comparison of the selfed generations S0 with S1, the fruit weight of the Lages population decreased by 0.380 g. There was also a reduction of 974.5 kg.ha-1 in the fruit yield of the Peruvian population. Thus, the performance of the P. peruviana populations in hybrid combinations is unpromising, indicating the existence of only one P. peruviana gene pool, with a restricted genetic basis.

Index terms
Physalis; combining ability; inbreeding depression; homozygosity

Resumo:

O melhoramento de Physalis peruviana é incipiente no Brasil e mostra-se como a alternativa mais promissora no desenvolvimento de genótipos produtivos e com qualidade de fruto. Sendo assim, o objetivo foi avaliar a capacidade de combinação entre linhagens endogâmicas de P. peruviana, indicando, assim, híbridos comqualidade de fruto. Para tanto, quatro populações de distintas origens (Colômbia, Lages,Caçador, Peru)foram submetidas a três gerações de autofecundação e a hibridação, totalizando28 genótipos. Utilizou-se um esquema de dialelo completo (Método 1 de Griffing) a fim de comparar o desempenho dos híbridos em relação aos genitores, com base nos efeitos dacapacidade geral e da capacidade específica de combinação. Os experimentos foramconduzidos em dois locais (Lages-SC e Xanxerê-SC), sob um delineamento de blocoscasualizados, com três repetições. Na análise de variância, o fator genótipo foi decomposto nasseguintes causas de variação: i) genitores e híbridos F1’s, ii) gerações de autofecundação e iii) interação genótipo x local. Houve diferenças significativas entre Genitores e híbridos F1’s parao caráter diâmetro polar do fruto. Foram observados valores significativos para adecomposição da interação: Capacidade específica x Local e Recíproco x Local. Porém, para oambiente de Xanxerê, houve redução de aproximadamente 3,0 mm no diâmetro polar do fruto,no híbrido Colômbia x Peru, e redução de 4,5 mm, para o recíproco (Peru x Colômbia). Comrelação às autofecundações, na comparação S0 vs. S1 para as populações Lages e Peru,houve redução na massa de frutos (0,380 g) e no rendimento de frutos (974,5kg.ha-1). Porém,de maneira geral, a qualidade de fruto não foi afetada em virtude dasautofecundações. As populações não manifestam desempenho promissor quando em combinações híbridas,revelando a existência de apenas um pool gênico de P. peruviana de restritabase genética.

Termos para indexação
Physalis; capacidade de combinação; depressão por endogamia; homozigose

Introduction

Physalis peruviana L. is a fruit species of Andean origin (MIRANDA; FISCHER, 2021 MIRANDA, D.; FISCHER, G. Avances tecnológicos en el cultivo de la uchuva (Physalis peruviana L.) en Colombia. In: FISCHER, G,; MIRANDA, D.; MAGNITSKIY, S.; BALAGUERA-LÓPEZ, H.; MOLANO, Z. Avances en el cultivo de las berries en el trópico. Bogotá: Sociedad Colombiana de Ciencias Hortícolas, 2021. p.14-36. ), and Colombia is the largest producer and exporter of fresh fruits, with a mean output of 16,4 t.ha-1 (AGRONET MINAGRICULTRA, 2019 AGRONET MINAGRICULTURA. Reporte: área, producción y rendimiento nacional por cultivo. Bogotá: Agronet Minagricultura, 2019. (Cadena de la uchuva).
https://www.agronet.gov.co/estadistica/P...
). The sensorial quality and beauty of the fruit are striking characteristics that explain the significant economic importance of P. peruviana. Moreover, the plant is diuretic and the leaf juice has been used in the treatment of worms and bowel complaints (IVANOVA et al., 2019 IVANOVA, T.; POPOVA, V.; MAZOVA, N.; STOYANOVA, A.; DAMYANOVA, S. Extratos de folhas de physalis (Physalis peruviana L.) para aplicação prospectiva em medicina e cosmética. Ukrainian Food Journal, Kyiv, n.8, p.34-44, 2019. Disponível em: http://nbuv.gov.ua/UJRN/UFJ_2019_8_1_5.
http://nbuv.gov.ua/UJRN/UFJ_2019_8_1_5...
). These properties make the crop even more attractive, since the search for nutritious foods with medicinal properties has nowadays become a priority (LAGOS-BURBANO et al., 2021 LAGOS-BURBANO, T.C.; MEJÍA-ESPAÑA, D.F.; ARANGO-BEDOYA, O.; VILLAQUIRÁN-SAMBONI, Z.Y.; LAGOS-SANTANDER, L.K.; DUARTE-ALVARADO, D.E. Propriedades físico-químicas de híbridos de groselha colombiana na seleção de materiais de alta qualidade. Pesquisa Agropecuária Brasileira, Brasília, DF, v.55, 2021. https://doi.org/10.1590/S1678-3921.pab2020.v55.01905.
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; BARROSO et al., 2022 BARROSO, N.D.S.; FONSECA, J.S.T.; RAMOS, C.A.D.S.; NASCIMENTO, M.N.D.; SOARES, T.L.; PELACANI, C.R. Impact of the maturity stage on harvest point of fruits and physiological quality of Physalis peruvianaL. seeds. Revista Brasileira de Fruticultura, Jaboticabal, v.44, p.e-848, 2022. https://doi.org /10.1590/0100-2945202284.
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).

In Brazil, P. peruviana is cultivated mostly in the southern region of the country (FISCHER et al., 2014 FISCHER, G.; ALMANZA-MERCHÁN, P.J.; MIRANDA, D. Importancia y cultivo de la uchuva (Physalis peruviana L.). Revista Brasileira de Fruticultura, Jaboticabal, v.36, p.1-15, 2014. https://dx.doi.org/10.1590/0100-2945-441/13.
https://dx.doi.org/10.1590/0100-2945-441...
). However, the current fruit production is insignificant in view of the demand of the consumer market (CEPA, 2020), and most of the sold fruit is imported. To make the country self-sufficient in fruit production, genotypes with superior fruit quality must be developed, prioritizing characteristics related to fruit size and flavor for the fresh market.

As observed in other species of the Solanaceae family, an efficient strategy for increasing fruit yield and quality is to explore the benefits of heterosis. Heterosis or hybrid vigor can be defined as the phenotypic difference between the hybrid progeny and the mean of the parents involved in the cross (HOCHHOLDINGER; BALDAUF, 2018 HOCHHOLDINGER, F.; BALDAUF, J.A. Heterosis in plants. Current Biology, London, v.28, n.18, p.R1089-R1092, 2018. ).

The phenomenon has aroused the interest of researchers for decades, but the causes for heterotic effects are still open questions.

Over the decades, different hypotheses were suggested, reasoning along different lines, explaining that heterosis is the result of: i) favorable allelic interactions caused by dominance and overdominance effects in different gene loci, and the genetic divergence between parents is the criterion used initially to manifestation this phenomenon (EAST, 1936 EAST, E.M. Heterosis. Genetics, Oxford, v.21, p.375-97, 1936. ); ii), more complex gene interactions, caused by epistatic interactions (WILLIAMS, 1959 WILLIAMS, W. Heterosis and the genetics of complex characters. Nature, London, v.184, n.4685, p.527, 1959. https://doi.org/10.1007/s00497-013-0237-4.
https://doi.org/10.1007/s00497-013-0237-...
; CHEN, 2013 CHEN, Z.J. Genomic and epigenetic insights into the molecular basis of heterosis. Nature Reviews Genetics, London, v.14, n.7, p.471-82, 2013. https://doi.org/10.1038/nrg3503.
https://doi.org/10.1038/nrg3503...
) and; iii) presence of biochemical- physiological stimuli (HOCHHOLDINGER; HOECKER, 2007 HOCHHOLDINGER, F.; HOECKER, N. Towards the molecular basis of heterosis. Trends in Plant Science, Amsterdam, v.12, n.9, p.427-32, 2007. https://doi.org/10.1016/j.tplants.2007.08.005.
https://doi.org/10.1016/j.tplants.2007.0...
; LI et al., 2020 LI, Z.; ZHU, A.; SONG, Q.; CHEN, H.Y.; HARMON, F.G.; CHEN, Z.J. Temporal regulation of the metabolome and proteome in photosynthetic and photorespiratory pathways contributes to maize heterosis. The Plant Cell, Rockville, v.32, n.12, p.3706-22, 2020. https://doi.org/10.1105/tpc.20.00320.
https://doi.org/10.1105/tpc.20.00320...
).

Although crosses between contrasting homozygous genotypes do not necessarily result in superior hybrid combinations, the use of inbred lines from different gene pools has been the basis for studies of genetic control (REIF; HALLAUER; MELCHINGER, 2005 REIF, J.C.; HALLAUER, A.R.; MELCHINGER, A. E. Heterosis and heterotic patterns in maize. Maydica, Bergamo, v.50, n.3/4, p.215, 2005. https://doi.org/10.2135/cssaspecpub25.c3.
https://doi.org/10.2135/cssaspecpub25.c3...
). The grouping of germplasm into heterotic groups or distinct gene groups contributes to the selection of adequate parents (MELCHINGER; GUMBER, 1998 MELCHINGER, A.E.; GUMBER, R.K. Overview of heterosis and heterotic groups in agronomic crops. In: KENDALL, R.; LARNKEY,J.E.S. Concepts and breeding of heterosis in crop plants. Madison: Crop Science Society of America, 1998. v.25. p.29-44. ). In general, crosses between lines of different gene groups perform better than crosses of lines of the same genetic base, because heterosis is a function of the differences between alleles donated by parents, involving non-additive interactions (MELCHINGER; GUMBER, 1998 MELCHINGER, A.E.; GUMBER, R.K. Overview of heterosis and heterotic groups in agronomic crops. In: KENDALL, R.; LARNKEY,J.E.S. Concepts and breeding of heterosis in crop plants. Madison: Crop Science Society of America, 1998. v.25. p.29-44. ; LI et al., 2022 LI, D.; L. U, X.; ZHU, Y.; PAN, J.; ZHOU, S.; ZHANG, X.; ZHANG, C. A base multi-ômica da heterose da batata. Journal of Integrative Plant Biology, Beiking, v.64, n.3, p.671-87, 2022. https://doi.org/10.1111/jipb.13211.
https://doi.org/10.1111/jipb.13211...
).

In Colombia, in the study by Fischer (1995 apud HERRERA; FISCHER; CHÁCON, 2012 HERRERA, A.M.; FISCHER, G.; CHÁCON, M. I. Agronomical evaluation of cape gosseberry (Physalis peruviana L.) from central and north-eastern Colombia. Agronomía Colombiana, Bogotá, v.30, p.15 -24, 2012. ) three genotypes (or ecotypes) were classified for differences in fruit size and flavor, according to their origin: Kenya, Southern Africa and Colombia. African genotypes are characterized by larger fruits (8 - 10 g), but have a lower sugar content and sugar/acidity ratio than the Colombian genotype, which has a mean fruit weight of 5 g (FISCHER; EBERT; LÜDDERS, 2007 FISCHER, G.; EBERT, G.; LÜDDERS, P. Production, seeds and carbohydrate contents of cape gooseberry (Physalis peruviana L.) fruits grown at two contrasting Colombian altitudes. Journal of Applied Botany and Food Quality, Go¨ttingen, v.81, n.1, p.29-35, 2007. ). Numerous accessions of the Colombian genotype were characterized and are currently maintained in gene banks (LAGOS; CRIOLLO; MOSQUERA 2001 LAGOS, T.C.; CRIOLLO, Y.C. MOSQUERA QUIJANO, C.A. Evaluación preliminar de cultivares de uvilla o uchuva (Physalis peruviana L.) para escoger materiales con base en la calidad del fruto. Revista de Ciencias Agrícolas, Pasto, v.18, n.2, p.82-94, 2001. ; BONILLA et al., 2008 BONILLA, M.K.; ESPINOSA, A.; POSSO, H.; VÁSQUEZ, J. MUÑOZ. Caracterización morfológica de 24 accesiones de uchuva del banco de germoplasma de la Universidad Nacional de Colombia, Sede Palmira. Acta Agronómica, Palmira, v.54, n.2, p.101-8. 2008. ; HERRERA, FISCHER; CHÁCON, 2012 HERRERA, A.M.; FISCHER, G.; CHÁCON, M. I. Agronomical evaluation of cape gosseberry (Physalis peruviana L.) from central and north-eastern Colombia. Agronomía Colombiana, Bogotá, v.30, p.15 -24, 2012. ). This represents a valuable genetic resource to be exploited in breeding programs, to develop new varieties as well as commercial hybrids. According to Leiva-Brondo et al. (2001) LEIVA-BRONDO, M.; PROHENS, J.; NUEZ, F. Genetic analysis indicate superiority of performance of P. peruviana (Physalis peruviana L.) hybrids. Journal of New Seeds, Binghamton, v.3 n.3, p.71-84, 2001. https://doi.org/10.1300/J153v03n03-04.
https://doi.org/10.1300/J153v03n03-04...
, when breeding P.peruviana for the development of commercial hybrids, one must consider the effects of dominant alleles on fruit quality traits. In the same sense, Lagos et al. (2005) LAGOS, T.C.; ESCOBAR, H.C.; PAREDES, O.; MORA, A.; VALLEJO, F.A. Estudio de la biologia floral de la uchuva (Physalis peruviana L.). Revista de Ciencias Agrícolas, Pasto, v.22, n.1, p.30-41, 2005. showed effects of specific combining ability - SCA in hybridizations of different P. peruviana accessions and, consequently, dominance effects on fruit yield components.

In Brazil, pioneering studies have shown that the selection and direct use of locally grown populations may not lead to satisfactory genetic gains (TREVISANI et al., 2016 TREVISANI, N.; SCHMIT, R.; MELO, R. C.; COIMBRA, J. L. M.; GUIDOLIN, A. F. Growth variation in reproductive structures of Physalis populations. Interciência, v. 41, n. 7, p. 470-475, 2016. ; SANTOS et al., 2023 SANTOS, M.D.; TREVISANI, N.; CERUTTI, P.H.; PIERRE, P.M.O.; GUIDOLIN, A.F. Origem, evolução e estratégias de melhoramento genético de physalis. Ciência Rural, Santa Maria, v.53, 2022. http://dx.doi.org /10.1590/0100-29452022848.
http://dx.doi.org /10.1590/0100-29452022...
). Therefore, two main strategies are currently being applied to broaden the genetic variability and selection of superior genotypes: mutation induction and, as the focus of this study, hybridization between populations of different origins, as a means to explore the benefits of heterosis in generation F1. In view of the above, the objective of the study was to evaluate the combining ability between P. peruviana parents to develop hybrid combinations with heterotic potential for fruit traits.

Material and methods

Origin of the P. peruviana populations

Four P. peruviana populations from different geographical regions (1- Colombia, 2 - Lages, 3 - Caçador, 4 - Peru) were classified as original (S0), i.e., populations established without pollination control, according to the natural reproduction mode of the species.

Five plants of each population were grown in a greenhouse (one plant per pots), and five random buds in the floral bud stage of each plant were protected with bags to prevent uncontrolled pollination. In this way, the inbreeding generation S1 of each original population was established.

The selfed generations were advanced with the same number of repetitions per population (five bagged buds/five plants), resulting in the inbreeding generations S2 and S3 of the four above populations. The selfing of the generations was also carried out in a greenhouse. This procedure resulted in 12 inbred populations, also called inbred lines, as shown in Figure 1.

Figure 1
Representative scheme of the P. peruviana populations, contemplating original populations, inbred lines and hybrids. In the hybridizations, the four populations (Lages, Colômbia, Caçador, Peru) were used in the third generation of self-fertilization (S3).

The four P. peruviana populations (Colombia, Lages, Caçador and Peru in the S3 generation) were crossed, using the inbred lines in generation S3. A full diallel mating design was used, with direct and reciprocal crosses and parents, which resulted in 12 F1 (six direct and six reciprocal) hybrid populations. After previous emasculation of the floral bud (removal of the stamens) of the female parent and manual application of male pollen, the flowers were hand-pollinated, as described in the Technical Manual for Controlled Crosses of P. peruviana L. In this way, 12 inbred populations, 12 hybrids and four original populations (without pollination control) were established, i.e., a total of 28 P. peruviana populations (Figure 1).

Experimental environment and design

The 28 P. peruviana populations were evaluated in two cultivation environments: i) county of Lages - SC (27º 48 ‘S and 50º 19’ W) on the highland plateau of Santa Catarina (Planalto Serrano Catarinense), at a mean altitude of 930 m asl, where the mean annual temperature is 14.6 °C. The soil is classified as Aluminum Leptic Cambisol Humic (properties: 34% clay; pH in water 5.93; acidity potential by the SMP method 5.21; 10.06 mg dm-3 P, 80 mg dm3 K; 2.61% OM; 5.42 cmol dm-3 Ca; and 2.10 cmol dm-3 Mg), with a moderate A horizon, clay texture and wavy relief and; ii) county of Xanxerê - SC (26º 48 ‘S and 52º 23’ O), in western Santa Catarina, at a mean altitude of 774 m asl and a mean annual temperature of 18.7 °C, on soil classified as Oxisol (properties: 45% clay, pH in water 5.82, potential acidity by the SMP method 6.01; 13.15 mg dm-3 P; 184.00 mg dm-3 K; 5.51% OM; 7.8 cmol dm-3 Ca; and 2.70 cmol dm-3 Mg).

The experiment was arranged in a randomized block design with three replications, in a factorial genotype × environment experimental design (28 x 2). The experimental unit consisted of five plants, at a spacing of 1 m between plants and 2 m between rows.

The five plants of each experimental unit were evaluated. Irrigations were carried out manually, according to the water needs of the crop. The recommendations for fertilization and phytosanitary control were made according to the recommendation for the tomato crop, which also belongs to the Solanaceae family.

Trait measurements

The seedlings were transplanted to the final planting environment in the second fortnight of December 2015. The evaluated traits were total fruit yield (FY - in kg.ha-1), mean fruit weight (MFW – in g), fruit polar diameter (PD – in mm), fruit equatorial diameter (ED – in mm), total soluble solids (TSS – in ° Brix) and total titratable acidity (TA - expressed as % citric acid). The traits PD, ED, TSS and TA were assessed twice (March and April) during the crop cycle. However, for the statistical data analysis, the mean of the evaluations was taken into consideration, due to the absence of variance between the periods.

The TSS contents were determined with a digital refractometer (model PR201α, Atago®), in an aliquot of processed fruit juice.

The TA values were measured in a 10-mL juice sample, diluted in 90 mL distilled water and titrated with 0.1 N sodium hydroxide solution to pH 8.1, using an automatic titrator TitroLine Easy®. Total acidity (TA) was expressed as % of citric acid, calculated by the formula below (where: n - volume of NaOH solution used for titration, in mL; N - normality of NaOH solution; Eq - equivalent-gram of acid; V - sample volume, in mL):

1 T A = n X N X E q 10 X V

Statistical analysis

The general statistical model contemplated a randomized block design in a factorial scheme: Yijk = overall mean + blocki + environment j + genotypek + environment*genotype jk + errorijk , where i = 1, 2, 3; j = 1,2; k = 1, 2, .., 28. From the general model, the mean squares were partitioned for the factors genotype and genotype × environment (GE) interaction, and the genotype factor (27 degrees of freedom) was subdivided into the following causes:

i) parents and F1 hybrids (15 degrees of freedom), partitioned into general combining ability (GCA), specific combining ability (SCA) and reciprocal effect (REC), determined by diallel analysis. The reciprocal effect (REC) was further partitioned into maternal (MAT) and non-maternal effects (NMAT).

ii) Generations of selfing (11 degrees of freedom).

iii) GE interaction (1 degree of freedom), partitioned into: parents and F1 hybrids * environment and selfed generations * environment.

The analysis of variance for the effects of GCA, SCA and reciprocal crosses was performed according to Griffing’s Method 1 (1956) (parents and direct and reciprocal hybrids), Model 1 (fixed genotype effects), for different environments. For the analysis, the SAS University Edition diallel (SAS05) program was used, described by Zhang, Kang and Lamkey (2005) ZHANG, Y.; KANG, M.S.; LAMKEY, K. R. Diallel-Sas05. Agronomy Journal, Madison, v.97, n.4, p.1097-106, 2005. https://doi.org/10.2134/agronj2004.0260. .

According to the proposed methodology, the model computed: Yijk = overall mean + gi + gj + sij + rij + lk + (gl)ik + (gl)jk + (sl)ijk + errorijk, where Yijk is the observation in the k-th environment for parents i and j; gi or gj are the GCA effect of parent i or j respectively, and corresponds to the deviation of its mean performance in hybrid combinations; sij is the SCA effect of the cross between parents i and j and shows whether their performance is higher or lower than expected based on the mean behavior of the parents involved; rij is the SCA effect expressed in the reciprocal cross between parents i and j; lk is the effect of environment k; (gl)ik and (gl)jk are the interaction between the GCA of parent i or j with environment k; (sl) ijk is the interaction between the SCA of cross ij with environment k and; (rl)ijk is the interaction between the SCA expressed in the reciprocal cross ij with environment k and; error ijk is the observation error. The estimates of GCA, SCA and reciprocal effect differed from zero and were tested by the Student’s t-test (ZHANG; KANG; LAMKEY, 2005 ZHANG, Y.; KANG, M.S.; LAMKEY, K. R. Diallel-Sas05. Agronomy Journal, Madison, v.97, n.4, p.1097-106, 2005. https://doi.org/10.2134/agronj2004.0260. ) at 5% probability.

To clarify the consequences of inbreeding, original populations (S0) and selfed generations generations (S1, S2, S3) were compared in univariate contrasts between the inbreeding generations of each P. peruviana population (Colombia, Lages, Caçador, Peru), resulting in 12 comparisons, according to the general model:

i) P. peruviana original population (S0) vs.first selfed generation (S1).

ii) P. peruviana population of first selfed generation (S1) vs. second selfed generation (S2).

iii) P. peruviana population of second selfed generation (S2) vs. third selfed generations (S3).

These contrasts were compared by the PROC GLM procedure of SAS. For each one, the differences between the means of interest were estimated to improve the interpretation of the results, by determining the occurrence as well as the level of inbreeding depression (function estimates). The differences between the means were compared by the Student’s t-test at 5% significance.

Results and discussion

The result of analysis of variance for the traits mean fruit weight (MFW) and fruit equatorial diameter (ED) differed between the evaluated genotypes (Table 1). The observed significance indicated the existence of genetic variability, resulting from additive and non-additive gene effects (FALCONER, 1987 FALCONER, D. S. Introdução à genética quantitativa. Viçosa: UFV, 1987. 279 p. ; THANH et al., 2010 THANH, N.M.; NGUYEN, N.H.; PONZONI, R.W.; VU, N.T.; BARNES, A.C.; MATHER, P.B. Estimates of strain additive and nonadditive genetic effects for growth traits in a diallel cross of three strains of giant freshwater prawn (Macrobrachium rosenbergii) in Vietnam. Aquaculture, Hoboken, v.299, n.1-4, p.30-6, 2010. https://doi.org/10.1016/j.aquaculture.2009.12.011.
https://doi.org/10.1016/j.aquaculture.20...
; FU et al., 2014 FU, D.; XIAO, M.; HAYWARD, A.; FU, Y.; LIU, G.; JIANG, G.; ZHANG, H. Utilization of crop heterosis: a review. Euphytica, Dordrecht, v.197, n.2, p.161-73, 2014. https://doi.org/10.1007/s10681-014-1103-7.
https://doi.org/10.1007/s10681-014-1103-...
). This information, which indicates the possibility of developing new cultivars or superior F1 hybrids, is fundamental for breeding programs.

Table 1
Analysis of variance for the traits fruit yield (FY), mean fruit weight (MFW), fruit polar diameter (PD), equatorial diameter (ED), total soluble solids (TSS) and total titratable acidity (TA), with the partitioning of the main population factor into: F1 parents and hybrids (GCA, SCA, REC, MAT, NMAT), the selfed generation factor and the interaction between the factors genotype × environment, with the respective degrees of freedom (DF) and mean squares (MS).

The genotype sums of squares were divided into two sources of variation, which were analyzed, namely: i) Parents and F1 hybrids for the GCA, SCA and reciprocal effects (DF 15); ii) Selfed generations (DF 11). Significant differences between parents and F1 hybrids for the fruit polar diameter (PD) indicate that the progenies may have a better or worse performance than the parents. Among the sources of variation related to the parents and F1 hybrids, the reciprocal effect was significant, suggesting the influence of maternal effects on PD, as shown by the mean square of MAT at 5% probability (Table 1).

The effect caused by the reciprocal cross was classified in maternal and non-maternal by Wu and Matheson (2001). WU, H.X.; MATHESON, A.C. Reciprocal, maternal and nonmaternal effects in radiata pine diallel mating experiment on four Australia sites. Forest Genetics, Zvolen, v.8, n.3, p.205-12, 2001. The maternal effect resulted from nuclear genes and the non-maternal (extrachromosomal inheritance) from genes located in cytoplasmic organelles (MUKANGA; DERERA; TONGOONA, 2010 MUKANGA, M.; DERERA, J.; TONGOONA, P. Gene action and reciprocal effects for ear rot resistance in crosses derived from five tropical maize populations. Euphytica, Dordrecht, v.174, n.2, p.293-301, 2010. https://doi.org/10.1007/s10681-010-0178-z.
https://doi.org/10.1007/s10681-010-0178-...
).

Therefore, a successful choice of P. peruviana lines for the development of hybrids with a larger PD depends on whether the parent is used as pollen donor or recipient. In case of maternal effects, the progeny phenotype is the expression of the maternal genotype in the first and, at most, in the second generation after the cross (NAVES et al., 2022 NAVES, E. R.; SCOSSA, F.; ARAÚJO, W. L.; NUNES-NESI, A.; FERNIE, A.R.; ZSÖGÖN, A. Heterose e efeitos recíprocos para características agronômicas e frutíferas em híbridos de pimenta Capsicum. Scientia Horticulturae , v. 295,p. 110821, 2022. ). In a study on the combining ability of 10 Physalis peruviana L. genotypes in Colombia, Lagos et al. (2007) LAGOS, T.; VALLEJO, F.; CRIOLLO, H. Combining ability analysis of some fruit traits of Physalis peruviana L. Agronomía Colombiana, Bogotá, v.25, n.1, p.36-46. 2007. found that for ED, the sums of squares of GCA and SCA were not-significant while the reciprocal effect was significant, indicating the relevance of the maternal component in the selection of this trait.

With regard to the effects of the combining ability in the environmental mean, the GCA was significant for fruit equatorial diameter (ED) (Table 1). This shows that at least one parent was superior to the others, based on its mean performance in hybrid combinations (PÁDUA et al., 2010 PÁDUA, T.R.P.D.; GOMES, L.A.A.; MALUF, W.R.; CARVALHO FILHO, J.L.S.D. Capacidade combinatória de híbridos de tomateiro de crescimento determinado, resistentes a Begomovirus e Tospovirus. Pesquisa Agropecuária Brasileira, Brasília, DF, v.45, p.818-25, 2010. https://doi.org/10.1590/S0100-204X2010000800007.
https://doi.org/10.1590/S0100-204X201000...
). The result indicates the importance of additive genetic variation in the expression of this quantitative trait, in the set of evaluated populations.

Consequently, the establishment of hybrids may not be the most promising strategy to increase ED. For the SCA on the other hand, no significant effect for any studied trait was observed, which shows that the hybrid combinations do not differ from each other in the mean of the environments. The coefficients of variation ranged from 7.41 to 33.71, considered of low magnitude. The inexpressive allelic complementarity of the parents in promoting loci with dominant and/or overdominant alleles was possibly due to the genetic similarities between the parents involved.

The determination of the predominant type of inheritance of quantitative traits is imperative for P. peruviana breeding, although few studies demonstrate the contribution of additive or dominant/overdominant genetic variance. In a pioneering study of Leiva- Brondo et al. (2001) LEIVA-BRONDO, M.; PROHENS, J.; NUEZ, F. Genetic analysis indicate superiority of performance of P. peruviana (Physalis peruviana L.) hybrids. Journal of New Seeds, Binghamton, v.3 n.3, p.71-84, 2001. https://doi.org/10.1300/J153v03n03-04.
https://doi.org/10.1300/J153v03n03-04...
with P. peruviana hybrids, a dominance/additivity ratio of > 1 for FY and FW per plant was observed, suggesting heterosis. In the greenhouse, the progenies performed better than the parents, with a mean FW of 1.91 g (parents) and 2.20 g (hybrids) (LEIVA-BRONDO et al., 2001 LEIVA-BRONDO, M.; PROHENS, J.; NUEZ, F. Genetic analysis indicate superiority of performance of P. peruviana (Physalis peruviana L.) hybrids. Journal of New Seeds, Binghamton, v.3 n.3, p.71-84, 2001. https://doi.org/10.1300/J153v03n03-04.
https://doi.org/10.1300/J153v03n03-04...
).

However, the magnitude of the values (difference of 0.29 g) may not be economically advantageous for the commercialization of hybrids. In the same sense, hybridizations with a view to exploring the benefits of heterosis among cultivated P. peruviana populations (Colombia, Lages, Caçador, Peru) may not be an efficient breeding strategy.

The additive gene interaction shows the high proportion of homozygous loci, which reinforces, among other factors, a high autogamy rate in P. peruviana. Nevertheless, the reproduction mode of Physalis is still a controversial issue. A significant number of scientific studies stated predominance of cross-fertilization in the species. According to Lagos et al. (2008) LAGOS, T.C.; VALLEJO, F.A.; CRIOLLO, H.; MUÑOZ, J.E. Biología reproductiva de la uchuva. Acta Agronómica, Palmira, v.57, p.81-8, 2008. , the mechanism of protogyny and the occurrence of heterostily favor allogamy.

Similarly, Chautá Melizzo et al. (2012 CHAUTÁ-MELLIZO, A.; CAMPBELL, S.A.; BONILLA, M.A.; THALER, J.S.; POVEDA, K. Effects of natural and artificial pollination on fruit and offspring quality. Basic and Applied Ecology, Jena, v.13, n.6, p.524-32, 2012. https://doi.org/10.1016/j.baae.2012.08.013.
https://doi.org/10.1016/j.baae.2012.08.0...
) observed that hand-selfing resulted in progenies with lower FY plant-1 and smaller fruits. On the contrary, Gupta and Roy (1981) GUPTA, S.K.; ROY, S.K. The floral biology of cape-gooseberry (Physalis peruviana L.). Indian Journal of Agricultural Science, New Delhi, v.51, p.353-5, 1981. emphasized the predominance of selfing in P. peruviana when conditions were unfavorable for cross-pollination. In this way, since the P. peruviana flower is hermaphrodite, pollination is likely to occur both by cross-fertilization as well as by selfing. This may be indicative that the species presents, that is, it is classified as an allogamous plant with frequent autogamy and with plasticity in the reproduction mode, depending on the environment.

According to the estimated GCA effects among the four studied P. peruviana populations, only the values of the Colombian population differed from zero (5% probability by the t-test) (Table 2). However, the results are not promising if populations with larger fruits are to be selected, since a reduction of 0.580 cm in PD and a reduction of 0.430 cm in ED of the fruit was observed, demonstrating the inferiority of the Colombian population in crosses with the other populations.

Therefore, it is evident that the hybridization between the gooseberry populations (Colombia, Lages, Caçador, Peru) may not be advantageous for satisfactory genetic gains, with a view to higher yields and improved gooseberry fruit quality.

Table 2
Estimates of the general combining ability (gi) for the traits fruit yield (FY - in Kg.ha-1), mean fruit weight (MFW - in g), fruit polar diameter (PD- in mm), fruit equatorial diameter (ED- in mm), total soluble solids (TSS- in ° Brix) and total titratable acidity (TA – in %) of four P. peruviana parents used in the diallel analysis.

When exploring the GE interaction, no significant effects were detected. However, the interaction between Parents and F1 × environment was significant for fruit polar diameter (PD) (Table 1). This shows variations in PD between the parents and hybrids, according to the environment of cultivation. When partitioning the interaction, the mean squares of the SCA × environment and REC × environment were significant. Thus, the SCA and REC effects were studied separately for each environment, to check the existence of hybrid combinations with a larger fruit diameter (ED). Among the hybrid combinations, for direct (Colombia vs. Peru) and reciprocal (Peru vs. Colombia) crosses there was a significant effect in Xanxerê. However, this effect was considered unfavorable for the selection of P. peruviana fruits, due to the PD reduction of approximately 3 mm (direct cross) and 4.5 mm (reciprocal) (Table 3).

Thus, the result reflects and reinforces the low combining ability of parents to promote superior progenies (Tables 1, 2and 3).

Table 3
Estimates of the specific combining ability (Sij) and reciprocal effect (rij) for the trait fruit polar diameter (PD-in mm) among four P. peruviana parents (from Colombia, Lages, Caçador and Peru) used in the diallel analysis, evaluated in Lages and Xanxerê.

The analysis of variance includes another important source of variation, resulting from the selfing generations, although no difference was observed between the P. peruviana populations in different selfed generations (Table 1). The contrast between parents and F1 vs.selfed generations was significant for MFW.

This suggests a possible difference between hybrids and inbred populations for this trait.

Therefore, original populations and selfed generations were specifically compared to quantify possible inbreeding effects, based on the mean of the environments.

The contrast estimates for FY in S0 vs. S1 and S1 vs. S2 showed differences in the Peruvian population (Table 4). Inbreeding effects were evidenced, with a FY reduction of approximately 970 kg.ha-1 fruits in the S1 generation.

Similarly, the MFW of the Lages population was approximately 400 mg lower in the comparison of S0 with S1.

Table 4
Differences between means for the traits fruit yield (FY), mean fruit weight (MFW), fruit polar diameter (PD), equatorial diameter (ED), total soluble solids (TSS), total titratable acidity (TA) in %, of four P. peruviana populations selfed (S0) and three generations (S1, S2, S3), in the mean of the environments (Lages and Xanxerê – SC).

As shown by Leiva-Brondo et al. (2001) LEIVA-BRONDO, M.; PROHENS, J.; NUEZ, F. Genetic analysis indicate superiority of performance of P. peruviana (Physalis peruviana L.) hybrids. Journal of New Seeds, Binghamton, v.3 n.3, p.71-84, 2001. https://doi.org/10.1300/J153v03n03-04.
https://doi.org/10.1300/J153v03n03-04...
and Chautá-Melizzo et al. (2012 CHAUTÁ-MELLIZO, A.; CAMPBELL, S.A.; BONILLA, M.A.; THALER, J.S.; POVEDA, K. Effects of natural and artificial pollination on fruit and offspring quality. Basic and Applied Ecology, Jena, v.13, n.6, p.524-32, 2012. https://doi.org/10.1016/j.baae.2012.08.013.
https://doi.org/10.1016/j.baae.2012.08.0...
), the results of this study reinforce the low magnitude of heterosis in hybrid combinations, as well as barely detectable inbreeding depression throughout the selfed generations. The high autogamy rate in P. peruviana may have contributed to the formation of pure lines, with high homozygosity. This result suggests that the exploitation of additive gene effects may be promising in physalis breeding. In summary, the common origin of the gooseberry populations and consequently restricted genetic base also contribute to an increase in inbreeding. Therefore, the currently cultivated gooseberry populations are believed to belong to the same gene pool, with limited genetic variability.

Since Colombia is the major producer and exporter of P. peruviana fruits (FISCHER et al., 2014 FISCHER, G.; ALMANZA-MERCHÁN, P.J.; MIRANDA, D. Importancia y cultivo de la uchuva (Physalis peruviana L.). Revista Brasileira de Fruticultura, Jaboticabal, v.36, p.1-15, 2014. https://dx.doi.org/10.1590/0100-2945-441/13.
https://dx.doi.org/10.1590/0100-2945-441...
; AGRONET MINAGRICULTURA, 2019 AGRONET MINAGRICULTURA. Reporte: área, producción y rendimiento nacional por cultivo. Bogotá: Agronet Minagricultura, 2019. (Cadena de la uchuva).
https://www.agronet.gov.co/estadistica/P...
), aside from the advances in gooseberry breeding in that country, prioritizing fruit traits, genotypes of worldwide cultivated P.peruviana were presumably derived from Colombian genotypes. This may have caused a drastic reduction in the genetic variability and the establishment of highly inbred populations.

The ease of seed purchase at local retail stores or even the exchange among rural producers are factors that facilitate P.peruviana cultivation in different regions.

In Brazil, no P. peruviana varieties are protected and/or registered by the Ministry of Agriculture, Livestock and Supply and, therefore, little is known about the genetic potential of cultivated populations.

Another factor worth mentioning is the ploidy level of this species. This factor may also have contributed to the low magnitude of inbreeding depression. P. peruviana comprises diploid (classified as “wild”) and tetraploid (classified as “cultivated”) genotypes (LIBERATO et al., 2014 LIBERATO, S.A.; SÁNCHEZ-BETANCOURT, E.; ARGÜELLES, J.H.; GONZÁLEZ, C.; NÚÑEZ, V.M. Citogenética de genotipos de uchuva, Physalis peruviana L., y Physalis floridana Rydb., con respuesta diferencial a Fusarium oxysporum. Corpoica Ciencia y Tecnologia Agropecuaria, Bogotá, v.15, n.1, p.51-61, 2014. https://doi.org/10.21930/rcta.vol15_num1_art:396.
https://doi.org/10.21930/rcta.vol15_num1...
). In Brazil, the cultivated populations are considered polyploid with tetraploid configuration (ARAÚJO et al., 2017 ARAÚJO, F.L.; QUEIROZ, S.R.D.O.D.; PASSOS, A.R.; OSUNA, J.T.A. Caracterização cromossômica em Physalis angulata L. e P. peruviana L. Magistra, Cruz das Almas, v.27, n.1, 82-9, 2017. ; TREVISANI et al., 2018 TREVISANI, N.; MELO, R.C.D.; PIERRE, P.M.O.; COLLI, M.P.; COIMBRA, J.L.M.; GUIDOLIN, A.F. Ploidy and DNA content of P. peruviana populations grown in southern Brazil. Caryologia, Oxford, v.71, n.4, p.414-9, 2018. https://doi.org/10.1080/00087114.2018.1494440.
https://doi.org/10.1080/00087114.2018.14...
). Therefore, given the inverse relationship between the ploidy level and the harmful effects of selfing on heterozygous loci, it is believed that polyploids express less marked inbreeding depression, for having multiple alleles at the same gene locus (LANDE; SCHEMSKE, 1985 LANDE, R.; SCHEMSKE, D. W. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution, Oxford, v.39, n.1, p.24-40, 1985. https://doi.org/10.1111/j.1558-5646.1985.tb04077.x
https://doi.org/10.1111/j.1558-5646.1985...
). It was evident that the four populations had a very similar performance over the generations (S1, S2, S3), with no reduction in the mean performance of most traits. Even for the quantitative traits, with a reduction of approximately 6% heterozygosity/locus in each generation, it is presumable that differences would be detected after three selfed generations, considering the reproduction mode by cross-fertilization.

With regard to the expression of heterosis, Washburn and Birchler (2014) WASHBURN, J.D.; BIRCHLER, J.A. Polyploids as a “model system” for the study of heterosis. Plant Reproduction, Berlin, v.27, p.1-5, 2014. defended the hypothesis that the heterosis of polyploid is superior to that of diploid organisms, due to their ability to contain greater allelic diversity, resulting from the combinations between the different alleles. In the same sense, Birchler et al. (2010 BIRCHLER, J. A.; YAO, H.; CHUDALAYANDI, S.; VAIMAN, D.; VEITIA, R A. Heterosis. The Plant Cell, Rockville, v.2, p. 2105-12, 2010. https://doi.org/10.1105/tpc.110.076133.
https://doi.org/10.1105/tpc.110.076133...
) used the term “progressive heterosis in autotetraploids”, i.e., the cross between four pure lines (for example, A× B and C× D), resulting in a double- cross hybrid (ABCD) with a high heterotic potential. According to Kaeppler (2012) KAEPPLER, S. Heterosis: many genes, many mechanisms and the search for an undiscovered unifying theory. ISRN Botany, New York, v.2012, 2012. https://doi.org/10.5402/2012/682824.
https://doi.org/10.5402/2012/682824...
, “progressive heterosis” is the increase in plant performance to the extent to which the probability of allelic diversity increases.

Therefore, the results reinforce the fact that the existence of a gene pool of cultivated P.peruviana with a restricted genetic base reduced the inbreeding and heterosis effects, even in polyploid organisms.

Therefore, the observed low inbreeding depression and low combining ability of parents to promote superior hybrid progenies reinforces some important aspects for P. peruviana breeding, e.g.: i) the plasticity of the species in terms of pollination mode, where variations in terms of a higher or lower allogamy/ autogamy rate may be influenced by environmental conditions. More, ii) the artificial selection processes at the locations of origin for traits of agronomic importance (fruit size, yield and flavor) as well as the predominant cultivation of tetraploid genotypes, due to their superior characteristics, were crucial for the restriction of the genetic base of the currently cultivated P. peruviana genotypes.

Conclusion

The performance of hybrid combinations of the P. peruviana populations grown in southern Brazil and of Andean origin is not promising for fruit traits, indicating a low heterotic potential caused by the genetic similarity between the populations. Low inbreeding depression was detected in the P. peruviana populations in the three selfed generations.

The expansion of the genetic base, be it by germplasm introduction or by mutation induction, is essential for the success of P. peruviana breeding in the southern region of Brazil.

Acknowledgements

The authors are indebted to the State University of Santa Catarina (UDESC), the Federal University of Santa Catarina (UFSC), the Federal University of Juiz de Fora (UFJF), the National Council for Scientific and Technological Development (CNPq), the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES) and Foundation for the Support of the Scientific and Technological Research of Santa Catarina (FAPESC) for the scholarship of one author and the financial support for the development of this study.

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Edited by

Willian Krause

Publication Dates

  • Publication in this collection
    15 Apr 2024
  • Date of issue
    2024

History

  • Received
    14 Mar 2023
  • Accepted
    06 Dec 2023
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