Enhancing parthenocarpy and fruit set in sugar apples through gibberellic acid induction

Melhorando a partenocarpia e a formação de frutos em pinheiras através da indução de ácido giberélico

Abstract:

In sugar apple cultivation, the implementation of manual pollination is imperative to enhance fruit set. However, this methodology concurrently leads to an elevation in seed count and in overall production expenses. As a potential solution, growth regulators have been employed across various crop types to augment fruit yield and to facilitate the development of seedless fruits. In order to achieve this goal, a range of concentrations (0, 250, 500, 750, and 1.000 mg L^-1) of gibberellic acid (GA₃) were administered to sugar apple trees during the flowering stage, specifically when the flowers were in the female phase. Subsequent applications were carried out at intervals of 7, 14, 21, and 35 days after the initial treatment, targeting already established fruits. After a span of thirteen weeks, the utilization of GA₃ exhibited multiple benefits. Notably, it led to a considerable increase in fruit set, reaching up to 75%. Furthermore, GA3 induced parthenocarpy in sugar apples, triggering fruit development without fertilization. Additionally, the application of GA₃ had a positive impact on key fruit attributes, including diameter, fresh weight, and soluble solids content. It is important to note, however, that the resultant fruits displayed a thicker peel and lower pulp content. Notwithstanding, the ratio of peel to pulp escalated proportionally with the concentration of GA₃ applied. To further enhance the physicochemical characteristics of sugar apples, it is recommended to explore doses exceeding 1.000 mg L^-1 as well as consider the synergistic effects achievable through a combination of different growth regulators. In conclusion, the outcomes unequivocally demonstrate that GA₃ induces parthenocarpy in sugar apples and effectively enhances fruit set.

Index terms
Annona squamosa L.; fruiting; GA₃; growth regulator

Resumo:

Na cultura da pinheira, a implementação da polinização manual é imperativa para aumentar a formação de frutos. No entanto, essa metodologia, simultaneamente, resulta em aumento na contagem de sementes e nos gastos gerais de produção. Como possível solução, reguladores de crescimento têm sido empregados em diversos tipos de culturas para aumentar o rendimento de frutos e facilitar o desenvolvimento de frutossem sementes.Para esse fim, uma gama de concentrações (0; 250; 500; 750 e 1.000 mg L^-1) de ácido giberélico (GA₃) foi administrada em árvores de atemoieira durante o estágiode floração,especificamente quando as flores estavam na fase feminina. Aplicações subsequentes foram realizadas em intervalos de 7; 14; 21 e 35 dias após o tratamento inicial,visando a frutos já estabelecidos. Após período de treze semanas, a utilização de GA₃ apresentou múltiplos benefícios. Notavelmente, resultou em aumento considerável na formação defrutos,atingindo até 75%. Além disso, o GA₃ induziu a partenocarpia na pinheira,desencadeando o desenvolvimento de frutos sem fertilização. Adicionalmente, a aplicação de GA₃ teve um impacto positivo em características-chave dos frutos, incluindo diâmetro, pesofresco e teor de sólidos solúveis. É importante notar, no entanto, que os frutos resultantesapresentaram casca mais espessa e menor teor de polpa. Não obstante, a relação casca/polpa aumentou proporcionalmente com a concentração de GA₃ aplicada. Para aprimorar ainda mais as características físico-químicas da atemoieira, é recomendável explorar dosesque excedam 1.000 mg L^-1, bem como considerar os efeitos sinérgicos alcançáveis através da combinação de diferentes reguladores de crescimento. Em conclusão, os resultados demonstram,inequivocamente,que o GA₃ induz a partenocarpia na atemoieira e, efetivamente, aumenta a formação de frutos.

Termos para indexação
Annona squamosa L.; frutificação; GA₃; regulador de crescimento

Introduction

Parthenocarpic fruits naturally develop when ovary growth occurs without pollination and/or fertilization, resulting in the absence of seed formation (TAKISAWA et al., 2017). The application of growth regulators to both pollinated and non-pollinated ovaries in various crop species has led to the conclusion that the initiation of fruit growth depends on hormones synthesized during ovary and/or seed development subsequent to pollination and fertilization.

Furthermore, auxins and gibberellins are recognized as the primary compounds involved in this process (SERRANI et al., 2010; TAIZ; ZEIGER, 2017).

Ordinarily, sugar apple trees (Annona squamosa L.) do not produce parthenocarpic fruits. However, a spontaneous mutant known as “seedless Thai” yields seedless fruits due to a defect in ovule development that results in failed seed formation (LORA et al., 2011). While such mutants are infrequent in natural occurrences, the desirability of seedless fruits is attributed to their ease of preparation and consumption by humans (ROYO et al., 2015).

In the context of natural pollination, sugar apple trees exhibit either low fruit set or the production of misshapen fruits (CAMPOS et al., 2004). These trees are pollinated by beetles through a cantharophilic process, but this type of pollination proves inefficient and is further compromised by insecticide application for pest control. Additionally, the protogynous dichogamy, where the gynoecium matures earlier than the androecium, along with the spatial separation of reproductive organs that inhibits self-pollination, contributes to a low pollination rate in sugar apple trees (KIILL; COSTA, 2003; KISHORE et al., 2012; HIWALE, 2015). Consequently, in sugar apple cultivation, manual pollination is conducted to ensure complete fertilization and the full development of carpels, resulting in improved fruit set and in the attainment of larger and more uniform fruits (RIBEIRO, 2006).

However, aside from demanding skilled labor for its execution, manual pollination augments seed count and production expenses (MOTA FILHO et al., 2012). Therefore, the utilization of growth regulators to induce the development of parthenocarpic fruits offers a potential alternative within the sugar apple cultivation context. In this study, the objective was to assess the effectiveness of gibberellic acid as an inducer of parthenocarpy in sugar apple trees.

Material and methods

The experiment took place in an experimental field located at 5°10’ S, 38°00’ W, and an altitude of 143 meters, between July 2014 and August 2015. Twenty sugar apple trees, each four years old and irrigated through micro-sprinklers, were meticulously selected and identified based on their uniformity, vigor, and health. This selection aimed at assessing the effects of applying gibberellic acid (GA₃) for the induction of parthenocarpy.

All plants underwent pruning to eliminate damaged branches or those showing symptoms of pest and disease attacks. After a 15-day interval, the plants were pruned to a height of 2 meters. Primary branches were shortened to lengths ranging between 40 and 60 centimeters, while secondary branches were shortened to lengths between 20 and 40 centimeters. Complete defoliation, starting from the apex and progressing towards the base, was carried out on all branches to encourage new growth (SANTOS et al., 2014).

Gibberellic acid (GA₃) was applied to the ovaries of five flowers from each plant at the female stage. Five different concentrations (0, 250, 500, 750, and 1.000 mg L^-1) of the commercial product Pro Gibb® 400 were utilized.

This product contains 40% (m m^-1) of gibberellic acid (GA3) in a dispersible granulate form.

A spray bottle applicator with a capacity of 500 ml was employed, delivering 1 ml of the gibberellic acid solution (equivalent to 1 spray) into the floral chamber between 5 and 9 a.m., a period of the day conducive to optimal pollen germination temperature (RODRIGUES et al., 2016). Subsequent applications were repeated at intervals of 7, 21, and 35 days after the initial application, targeting the pre-existing fruits. Special care was taken to ensure complete coverage of the entire fruit with the solution.

Fruit set was assessed on a weekly basis, starting from the 7th day following the first application of the regulator and continuing until harvest, which occurred 93 days after anthesis. Additionally, every 14 days, the longitudinal and equatorial diameters of the fruits were measured using a digital caliper.

The equatorial diameter was measured by positioning the caliper at the center of the fruit. The effectiveness of fruiting was evaluated at harvest, marked by carpel separation and a yellow-green coloration observed in the intercarpelar tissues (PEREIRA et al., 2010).

Upon harvesting, fruits were placed in plastic boxes and transported to the laboratory for quality assessments. Measurements were taken for fresh weight, longitudinal and equatorial diameters of the fruits.

Subsequently, peel, peduncle, and pulp were separated to determine their respective weights. Fruit pulp was then analyzed for soluble solids content using an ATAGO bench refractometer, with the values expressed as a percentage.

A randomized block design featuring 4 replicates (4 plants per treatment) was employed for each concentration of gibberellic acid (0, 250, 500, 750, and 1.000 mg L^-1). The collected data underwent analysis of variance using the F test (p<0.05), and the impacts of gibberellic acid concentration were further examined through regression analysis (p<0.05). All statistical analyses were conducted using R software version 3.4.2.

Results and discussion

GA₃ induced parthenocarpy and enhanced fruit set in sugar apple trees. The highest level of fruit set (75%) was achieved with the 1.000 mg L^-1 GA₃ dosage, which was 2.5 times greater than the fruit set achieved with 250 mg L^-1 (Figure 1A). Conversely, no fruit set was observed with the 0 mg L^-1 dosage.

Assessing fruit development over time, the 1.000 mg L^-1 GA₃ treatment initially resulted in a fruit set of 95%, which exhibited a slight reduction until harvest. In contrast, when lower GA₃ concentrations were used (250 mg L^-1), a significant decline in fruit set occurred during the second week after anthesis, dropping from 95% to 30% (Figure 1B).

Figure 1
Fruit set of sugar apples (Annona squamosa L.) at harvest time (A; 93 days after anthesis) and over time (B). Plants were treated with gibberellic acid (0, 250, 500, 750, and 1.000 mg L^-1GA₃) on flowers in the female stage and at 7, 14, 21, and 35 days on pre-established fruits. Bars represent the standard error of the mean (n = 20) (Limoeiro do Norte-CE, 2015).

Figure 2
Size and width of a parthenocarpic sugar apple fruit. The authors' personal archives.

Moreover, GA₃ treatment displayed a linear improvement in both polar (34%) and equatorial (44%) fruit diameters in sugar apples (Figure 2 and 3A). Furthermore, evaluating the progression over time, a rapid increase in fruit size was observed with higher GA3 doses (Figure 3B and 3C).

Figure 3
Fruit diameter of sugar apples (Annona squamosaL.) at harvest time (A; 93 days after anthesis) and over time (B and C). Plants were treated with gibberellic acid (0, 250, 500, 750, and 1.000 mg L^-1 GA₃) on flowers in the female stage and at 7, 14, 21, and 35 days on pre-established fruits. Bars indicate the standard error of the mean (n = 20) (Limoeiro do Norte-CE, 2015).

GA₃ application also resulted in a significant increase in the fresh weight of sugar apples.

Notably, the 1.000 mg L^-1 dosage led to a 135% increase in fresh weight compared to the 250 mg L^-1 dosage (Figure 4A). Nevertheless, it is worth noting that the peel constituted approximately 67% of the total fruit weight.

Figure 4
Fresh weight and fruit components of sugar apples (Annona squamosa L.) at harvest time (93 days after anthesis). The plants were subjected to gibberellic acid treatment (0, 250, 500, 750, and 1.000 mg L^-1 GA₃) during the flowering stage and at 7, 14, 21, and 35 days on pre-established fruits. The error bars represent the standard error of the mean (n = 20) (Limoeiro do Norte-CE, 2015).

Fresh weight and soluble solids were higher as the concentration of GA₃ applied increased, with maximum values of 200.7 g and 19.21%, respectively (Figure 5).

Figure 5
Soluble solids and titratable acidity of sugar apples (Annona squamosa L.) at harvest time (93 days after anthesis). Plants were treated with gibberellic acid (0, 250, 500, 750, and 1000 mg L^-1 GA₃) on flowers in the female stage and at 7, 14, 21, and 35 days on pre-established fruits (Limoeiro do Norte-CE, 2015).

This demonstrates that the exogenous application of GA₃ promoted fruit retention and reduced fruit abortion. A higher percentage of fruit retention and consequently a lower abortion rate were observed with the application of higher concentrations of GA₃. This phenomenon can be attributed to gibberellin’s characteristic of inducing auxin formation by stimulating the synthesis of proteolytic enzymes that can release tryptophan, an auxin precursor. Auxin is the phytohormone responsible for fruit retention and development (WANG et al., 2009).

In naturally pollinated fruits, auxin is synthesized in the seed endosperm and exported to the fruit, promoting an increase in mesocarp volume and consequent fruit establishment (SILVA et al., 2011). However, in sugar apples, natural pollination results in low fruit retention, with rates as low as 7.6% (SANTOS et al., 2014). With such a low rate of pollination, seed development does not occur.

Without the necessary auxin source to facilitate fruit retention, abscission takes place (PEREIRA et al., 2014). In this context, the exogenous application of GA₃ could have acted as an inducer of auxin production, thereby facilitating fruit retention in this study, even in the absence of seed formation(Figure 6).

Figure 6
Parthenocarpic sugar apple fruit. The authors' personal archives.

Consequently, the application of gibberellic acid to female flowers holds promise for enhancing fruit retention in sugar apples. Similar results were observed with the ‘Gefner’ atemoya (Annona cherimola Mill x Annona squamosa L.) in Minas Gerais, where treatment with 1.000 mg L^-1 GA3 also yielded seedless fruits with a retention rate of 85%, 19 weeks after the regulator application (PEREIRA et al., 2014).

These findings aligned with the fruit diameters of various sugar apple genotypes cultivated in Bom Jesus, Piauí (CAVALCANTE et al., 2011). The authors reported longitudinal and equatorial diameters averaging 60.9 mm and 68.3 mm, respectively. These results underscore the role of gibberellin in fruit growth, as cell division and elongation hinge on a delicate balance between auxin, cytokinin, and gibberellin (JONG et al., 2009).

Fresh weight exhibited superiority, and soluble solids showed resemblance to the results obtained by Cavalcante et al. (2011), who recorded averages ranging from 103.1 g to 193.8 g and from 15.3% to 21.0%, respectively, across different sugar apple genotypes. Regarding pulp content, no significant differences emerged based on the applied GA₃ dose. On average, the fruits contained 20.8% of pulp in relation to the weight of the fruit, including peel and peduncle.

Conclusion

Parthenocarpic sugar apple fruits can be achieved through the application of gibberellic acid to female flowers. The dosage of 1.000 mg L^-1 of gibberellic acid yields retention rates, weight, size, and soluble solids content in alignment with commercial standards, albeit with a low pulp-to-peel ratio.

Higher doses of gibberellic acid should be investigated to assess potential increases in fruit production and retention.

References

• CAMPOS, R.D.S.; EURICO, E.D.L.; OLIVEIRA, J.D.; FONSECA, F.D.; SANTIAGO, A.D.; BARROS, P.G. Polinização natural, manual e autopolinização no pegamento de frutos de pinheira (Annona squamosa L.) em Alagoas. Revista Brasileira de Fruticultura, Jaboticabal, v.26, n.2, p.261-3, 2004. https://doi.org/10.1590/S0100-29452004000200020
  » https://doi.org/10.1590/S0100-29452004000200020
• CAVALCANTE,I.H.L.; MOURA, M.C.S.D.; ROCHA, L.F.D.; JÚNIOR, S.; MARTINS, L.D.V.; SILVA, R.R.S.D. Seleção preliminar de genótipos de pinheira em Bom Jesus-PI. Revista de Ciências Agrárias, Lisboa, v.34, p.173-81, 2011. https://doi.org/10.19084/rca.15940
  » https://doi.org/10.19084/rca.15940
• HIWALE, S. Custard apple (Annona squamosa L.). In: HIWALE, S. Sustainable horticulture in semiarid dry lands New Delhi: Springer, 2015. p.135-52.
• JONG, M.; MARIANI, C.; VRIEZEN, W.H. The role of auxin and gibberellin in tomato fruit set. Journal of Experimental Botany, Oxford, v.60, p.1523-32, 2009. https://doi.org/10.1093/jxb/erp094
  » https://doi.org/10.1093/jxb/erp094
• KIILL, L.H.P.; COSTA, J.G. Biologia floral e sistema de reprodução de Annona squamosa L. (Annonaceae) na região de Petrolina-PE. Ciência Rural, Santa Maria, v.33, p.851-6. 2003. https://doi.org/10.1590/S0103-84782003000500009
  » https://doi.org/10.1590/S0103-84782003000500009
• KISHORE, K.; SHUKLA, A.K.; BABU, N.; SARANGI, D.N.; PATANAYAK, S. Pollination biology of Annona squamosa L. (Annonaceae): Evidence for pollination syndrome. Scientia Horticulturae, New York, v.144, p.212-7, 2012. https://doi.org/10.1016/j.scienta.2012.07.004
  » https://doi.org/10.1016/j.scienta.2012.07.004
• LORA, J.; HORMAZA, J.I.; HERRERO, M.; GASSER, C.S. Seedless fruits and the disruption of a conserved genetic pathway in angiosperm ovule development. PNAS, Oxford, v.108, p.5461-5, 2001. https://doi.org/10.1073/pnas.1014514108
  » https://doi.org/10.1073/pnas.1014514108
• MOTA FILHO, G.; JAMIR, V.; TOLEDO PEREIRA, M.C.; NIETSCHE, S.; RODRIGUES GUIMARÃES, J.F.; ROCHA MOREIRA, G.B.; PRATES FERNANDES, T. Uso de fitorreguladores no desenvolvimento de frutos na atemoieira (Annona cherimola x A. squamosa cv. Gefner). Revista Ceres, Viçosa, MG, v.59, p.636-45, 2012. https://doi.org/10.1590/S0034-737X2012000500009
  » https://doi.org/10.1590/S0034-737X2012000500009
• PEREIRA, M.C.T.; BRAZ, L.C.; NIETSCHE, S.; MOTA, W.F. da. Determining the harvest maturity of the sugar apple fruits on northern Minas Gerais. Acta Horticulturae, The Hague, v.864, p.207-14, 2010. https://doi.org/10.17660/ActaHortic.2010.864.27
  » https://doi.org/10.17660/ActaHortic.2010.864.27
• PEREIRA, M.C.T.; SANTOS, R.K.A.; NIETSCHE, S.; MIZOBUTSI, G.P.; DOS SANTOS, E.F. Doses de ácido giberélico na frutificação efetiva e qualidade de frutos de atemoieira 'Gefner'. Revista Brasileira de Fruticultura, Jaboticabal, v.36, nesp, p.184-91, 2014. https://doi.org/10.1590/S0100-29452014000500022
  » https://doi.org/10.1590/S0100-29452014000500022
• RIBEIRO, G.S. Aspectos da biologia floral relacionados à produção de sementes e frutos de pinha (Annona squamosa L.) 2006. 67f. Dissertação (Mestrado) – Universidade Estadual do Sudoeste da Bahia, Vitória da Conquista, 2006.
• RODRIGUES, B.R.A.; SANTOS, R.C.D.; NIETSCHE, S.; MERCADANTE-SIMÕES, M.O.; CUNHA, I.R.G.D.; PEREIRA, M.C.T. Determination of cardinal temperatures for sugar apple (Annona squamosa L.). Ciência e Agrotecnologia, Lavras, v.40, n.2, p.145-54, 2016. https://doi.org/10.1590/1413-70542016402039115
  » https://doi.org/10.1590/1413-70542016402039115
• ROYO, C.; CARBONELL-BEJERANO, P.; TORRES-PÉREZ, R.; NEBISH, A.; MARTÍNEZ, Ó.; REY, M.; AROUTIOUNIAN, R.; IBÁÑEZ, J.; MARTÍNEZ-ZAPATER, J.M. Developmental, transcriptome, and genetic alterations associated with parthenocarpy in the grapevine seedless somatic variant Corinto bianco. Journal of Experimental Botany, Oxford, v.67, p.259-73, 2015. https://doi.org/10.1093/jxb/erv452
  » https://doi.org/10.1093/jxb/erv452
• SANTOS, P.C.; NOGUEIRA, A.S.; FREITAS, M.S.M.; FREITAS, J.A.A.; CARVALHO, A.J.C. de. Influência da época de poda e tipos de polinização no florescimento e frutificação da pinha. Revista Brasileira de Fruticultura, Jaboticabal, v.36, p.192-201, 2014. https://doi.org/10.1590/S0100-29452014000500023
  » https://doi.org/10.1590/S0100-29452014000500023
• SERRANI, J.C.; CARRERA, E.; RUIZ-RIVERO, O.; GALLEGO-GIRALDO, L.; PERES, L.E.; GARCIA-MARTINEZ, J.L. Inhibition of auxin transport from the ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins. Plant Physiology, Lancaster, v.110, p.110-55, 2010. https://doi.org/10.1104/pp.110.155424
  » https://doi.org/10.1104/pp.110.155424
• SILVA, J. A. T.; POERWANTO, R.; SOESANTO, S. Indole-3-acetic acid, 1-amino cyclopropane-1-carboxylic acid, and carbohydrate in relation to fruit drop on mango tree. Journal of Fruit and Ornamental Plant Research, Skierniewice, v.19, p.41-9, 2011.
• TAIZ, L.; ZEIGER, E. Fisiologia vegetal Porto Alegre: Artmed, 2013. 953 p.
• TAKISAWA, R.; MARUYAMA, T.; NAKAZAKI, T.; KATAOKA, K.; SAITO, H.; KOEDA, S.; NUNOME, T.; FUKUOKA, H.; KITAJIMA, A. Parthenocarpy in the tomato (Solanum lycopersicum L.) cultivar ‘MPK-1’is controlled by a novel parthenocarpic gene. The Horticulture Journal, Kyoto, v.86, n.4, p.487-92, 2017. https://doi.org/10.2503/hortj.OKD-042
  » https://doi.org/10.2503/hortj.OKD-042
• WANG, H.; SCHAUER, N.; USADEL, B.; FRASSE, P.; ZOUINE, M.; HERNOULD, M.; LATCHÉ A.; PECH, J.C.; FERNIE, A.R.; BOUZAYEN, M. Regulatory features underlying pollination-dependent and independent tomato fruit set revealed by transcript and primary metabolite profiling. The Plant Cell, Rockville v.21, n.5, p.1428-52, 2009. https://doi.org/10.1105/tpc.108.060830
  » https://doi.org/10.1105/tpc.108.060830

Edited by

• Juliana Domingues Lima

Publication Dates

• Publication in this collection
  09 Dec 2024
• Date of issue
  2024

History

• Published
  13 Nov 2024
• Received
  20 Feb 2024
• Accepted
  18 July 2024