Estimating Maternal Effects on Yield Traits in F 1 Hybrids of Tomato (Solanum lycopersicum) Using a Modified Diallel Cross Model

doi:10.21203/rs.3.rs-3954431/v1

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Estimating Maternal Effects on Yield Traits in F 1 Hybrids of Tomato (Solanum lycopersicum) Using a Modified Diallel Cross Model

https://doi.org/10.21203/rs.3.rs-3954431/v1

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This study aimed to compare the effects of General Combining Ability (GCA) and Specific Combining Ability (SCA) before and after partitioning, and to assess each parent's contribution to its cross combination while detecting the significance of maternal effects on tomato fruit traits. Three tomato lines were crossbred in a 3 x 3 diallel cross design to produce F1 hybrids, which were evaluated alongside their respective parents using a Randomized Complete Block Design with four replications. Findings revealed that GCA effects estimated through Griffing’s method were consistent with the average GCA effects of each parent after partitioning in the proposed model. Additionally, the difference between female and male GCA effects provided a reliable estimation of maternal effects, particularly for additive alleles, as corroborated by Hayman analysis for traits such as seed number, weight, and yield. SCA effects calculated through Griffing’s method mirrored the average SCA effects of each cross and its reciprocal, while the proposed model showed that the difference between SCA effects of each cross and its reciprocal equaled reciprocal effects, demonstrating the precise estimation of reciprocal effects in capturing the interaction between nuclear and cytoplasmic genes in the cross and its reciprocal hybrid.

Maternal effects

Combining ability

Diallel cross

Tomato

Solanum lycopersicum

Tomato (Solanum lycopersicum. L), is one of the most consumed vegetables globally due to its status as a basic ingredient in a large variety of raw or processed foods and an annual production of about 170 million tons (FAO, 2014). It belongs to the family Solanaceae, which includes more than 3000 species (Fentik, 2017). Tomato plays a significant role in human nutrition and its production is considered one of the main agricultural enterprises as it employs people in farms, processing industries and provides higher income per hectare to small holder farmers than most staple crops (Naika et. al., 2005). Tomato is not only considered as an economically important crop, but it is also a model plant species, due to its diploid, relatively compact, and recently sequenced genome, as well as its large genetic and genomic resources (Ranjan et. al., 2012).

The success of genetic advancements in cultivating desired traits in crop plants relies heavily on understanding the nature and extent of genetic variability and interactions inherent in the trait inheritance process (Ghareeb and Fares, 2016). To gain valuable insights into the genetic behavior of these traits in the first generation (F₁), the diallel cross technique is employed (Chowdhry et al., 1992). This technique offers early insights into the genetic dynamics of these traits and has the potential to generate novel genetic combinations, potentially surpassing the performance of the parental lines. It is essential to note that parental superiority may not solely hinge on their individual performances but also on their adeptness in combining effectively and producing transgressive segregants (Zhang and Kang, 1997).

The impact of parental environments on the phenotypes of offspring often constitutes an overlooked pathway within organismal life histories (Badyaev and Uller, 2009). Nevertheless, this pathway plays a crucial role in completing the life cycle, forging a connection from one generation to the next. Maternal effects represent a distinctive form of phenotypic plasticity, encapsulating the developmental interdependence of later life stages on earlier ones. In the context of maternal effects, the phenotypes of offspring undergo modification based on the environment shaped or encountered by the maternal parent. Specifically, 'maternal environmental effects' denote the phenomenon by which the external ecological conditions surrounding the maternal parent exert an influence on the phenotype of its progeny (Donohue, 2009).

The consideration of combining ability holds paramount importance for plant breeders, providing a valuable criterion for testing procedures aimed at studying and comparing the performance of lines in hybrid combinations and understanding the nature of gene action. Plant breeders are keenly interested in gene effect estimates, as these play a crucial role in determining the most effective breeding procedures for enhancing desired attributes. The selection of an optimal breeding methodology is largely contingent upon the type of gene action governing the genetic behavior of various agronomic and economic traits (Begna, 2021).

Griffing (1956) introduced the concept of diallel crosses, a technique widely employed in plant breeding. However, the determination of general and specific combining ability effects often relies on the average impact of a parent when utilized as either a female or a male in hybrid combinations, assuming their effects are comparable, as suggested by Yates (1947). In fixed models incorporating crosses and their reciprocals, only one general combining ability (GCA) effect value for each parent and one specific combining ability (SCA) effect value for each cross combination are estimated. Unfortunately, these estimated effects remain undifferentiated, failing to illuminate the unique contributions of each parent to the cross combination when employed as a male or female.

The distinction between the interaction effect of the cross and its reciprocal primarily arises from the interplay between nuclear and cytoplasmic genes. The cytoplasm of the female parent may represent a distinct environment that varies from one parent to another (Ghareeb et. al., 2014), thereby interacting differently with nuclear genes. To gain more comprehensive insights, the partitioning of general and specific combining ability effects becomes imperative, offering additional information about each parent when used as a female or a male in hybrid combinations (Mahgoub, 2004). Enhancing the precision of the statistical model used for estimating GCA and SCA effects serves as a valuable tool for selecting breeding methods and paired populations in reciprocal recurrent selection programs. Therefore, the objectives of the present study was to compare GCA and SCA effects and assess the relative contribution of each parent to its cross combination with a view to detecting the significance of maternal effects.

Genetic Materials and Cross Model

The experiments were conducted at the Department of Crop Science Research Farm, University of Nigeria, Nsukka, situated at latitude 0.6⁰52N, longitude 07⁰24E, and an altitude of 447.26m above sea level. The materials utilized in this study included a widely recognized tomato variety, Cobra (CB) and two tomato mutants, MA and MB, generated within the tomato breeding program of the Department of Crop Science, University of Nigeria, Nsukka.

Seeds of the three tomato lines were sown in nursery boxes filled with compost manure to facilitate seedling growth. Hybridization involved all possible combinations among the different lines. Successfully crossed plants were harvested and treated individually. Subsequently, the seeds were sown to generate the F₁ hybrids resulting from the various crosses. The six F₁ hybrids and their respective parental lines were nurtured in nursery boxes to promote seedling growth. Transplanting was done four weeks after planting. The experimental design was a Randomized Complete Block Design (RCBD) with four replications. Each entry was cultivated in single rows, with five plants in each row, utilizing inter-row spacing of 60cm and intra-row spacing of 45cm.

Data were collected on days to fruiting, days to fruit ripening, number of trusses per plant, number of fruits per truss, mean fruit weight per plant (g), harvest duration (days), and shelf life (days).

Statistical Analysis

An analysis of variance was conducted to assess the significance of genotypic differences. Having established significant differences among the genotypes, the total variance was dissected into genetic factors using two partitioning methods. Griffing's Model (1956) Method 1, in a modified form, was applied. This involved the partitioning of General Combining Ability (GCA) and Specific Combining Ability (SCA) effects. The essence was to assess the unique contribution of each parent when utilized as a male or a female in hybrid combinations. Unlike the conventional method that considers the average performance of male and female parents, this modification, as proposed by Mahgoub (2011), allowed for a more nuanced understanding of the parental contributions in specific hybrid combinations.

Proposed Model Formula

Griffing's method 1 model I, incorporating parents (P), F₁ hybrids, and their reciprocals, was employed with various effects estimated as per Griffing (1956):

ĝ _i = \(\left(\frac{1}{2p}\right)\)(x_i. + x._i) - \(\left(\frac{1}{p2}\right)\)x..,

ŝ _ij = \(\left(\frac{1}{2}\right)\) (x_ij + x_ji) – \(\left(\frac{1}{2p}\right)\) (x_i. + x._i + x_j. + x._j) \(+ \left(\frac{1}{p2}\right)\) x..,

ȓ _ij = \(\left(\frac{1}{2}\right)\) (x_ij + x_ji).

Maternal effect, following Cockerham (1963) and using Griffing's notations, is calculated as:

ḿ = \(\left(\frac{xi. +x.j}{2p}\right)\)

where x_i.: is the sum of the ith female over all males; x._i: is the sum of the ith male over all females; x_j.: is the sum of the jth female over all males; x._j: is the sum of the jth male over all females; x_ij: is the mean for the F₁ resulting from crossing the ith female and the jth male parents, x_ji: is the mean for the F₁ resulting from crossing the _jth female and the _ith male parents; ĝ_i: is the general combining ability effect of the ith parent, ŝ_ij: is the specific combining ability effect for the cross between the ith female and the jth male parents (ŝ_ij = ŝ_ji), ȓ_ij: is the reciprocal effect involving the ith and jth parents, ḿ_i: is the maternal effect of the ith parent and x..: is the grand total.

For proposed model where GCA effect (ĝ_i) is partitioned to estimate GCA effect for the parent when it is used as a female in its hybrid combination (ĝ_fi), and GCA effect for the same parent when it is used as a male in its hybrid combination (ĝ_mi) as follows:

ĝ _fi = \(\left(\frac{1}{p}\right)\) (x_i.) - \(\left(\frac{1}{p2}\right)\) x..,

ĝ _mi = \(\left(\frac{1}{p}\right)\) (x._i) - \(\left(\frac{1}{p2}\right)\) x..,

where ĝ_fi: is the deviation of the mean performance of the ith parent when it is used as a female, averaged over a set of P males, from the grand mean and ĝ_mi: is the deviation of the mean performance of the ith parent when it is used as a male, averaged over a set of P females, from the grand mean where:

ĝ _i = \(\left(\frac{1}{2}\right)\) (ĝ_{fi +} ĝ_mi) and, ḿ = \(\left(\frac{1}{2}\right)\) (ĝ_{fi −} ĝ_mi).

This proves that the average of the difference between ĝ_fi and ĝ_mi is exactly equal to maternal effect (ḿ). In other words, estimation of (ĝ_fi - ĝ_mi) would provide precise estimation for the maternal effect. General combining ability effect provides estimation for the additive effect. Therefore, maternal effect is mainly additive and expresses how much additive effect is involved.

Specific combining ability effect is partitioned to estimate SCA effect for the cross ŝ_ij and for its reciprocal ŝ_ji as follows:

ŝ _ij = x_ij - \(\left(\frac{1}{2p}\right)\) (x_i. + x._i + x_j. + x._j) + \(\left(\frac{1}{p2}\right)\) x..,

ŝ _ji = x._ji - \(\left(\frac{1}{2p}\right)\) (x_i. + x._i + x_j. + x._j) + \(\left(\frac{1}{p2}\right)\) x..,

Where the average of the partitioned components (ŝ_ij and ŝ_ji) is equal to calculated ŝ_ij according to Griffing’s method, ŝ_ij: is the SCA effect of the ith female and the jth male parent, and ŝ_ji is the SCA effect of the reciprocal and the jth female and the ith male parent

The advancement in the breeding program of specific crop characteristics is contingent upon the variability within populations and the heritability of desirable traits. Understanding the genetic foundation of traits, particularly yield, is crucial for formulating effective breeding strategies to enhance genotypic performance. Consequently, the ensuing discussion will elucidate the obtained results and their implications for tomato breeding programs.

General Combining ability

The estimates of GCA effects ‘‘ĝ_i” are listed in Table 1, where it differed from one parent to another and from character to other. Partitioning of the GCA effects to estimate male ‘‘ĝ_mi” and female ‘‘ĝ_fi” effects revealed that their average values equal calculated value according to Griffing’s method ‘‘ĝ_i”. The difference between ĝ_fi and ĝ_mi revealed that the GCA effect estimates ‘‘ĝ_i” might underestimate the value of the parent, then values of ĝ_fi and ĝ_mi showed better performance in its hybrid combinations.

In the pursuit of refined crop traits through selective breeding, a nuanced examination of the General Combining Ability (GCA) effects, segregated into female (ĝfi) and male (ĝmi) contributions, unveils the distinctive roles played by the three parent varieties - CB, MA, and MB across a range of tomato fruit traits.

The CB variety unfolds intricate patterns in its GCA effects. For days to fruiting and fruit ripening, the female parent (ĝfi) made positive contributions of 0.37 and 1.54, respectively, suggesting a favorable impact on fruiting characteristics. Conversely, the male parent (ĝmi) exhibited negative effects of -0.73 and − 0.66, indicating a contrasting influence. These trends extend to other traits such as number of trusses per plant (-1.28 and 0.26), mean fruit weight (-3.93 and 0.77), harvest duration (0.40 and 0.51), and shelf life (1.36 and 0.26) for ĝfi and ĝmi, respectively. The marked differences underscore the need to consider both parents for a nuanced approach to trait-specific breeding strategies.

Similar to CB, MA exhibited distinct GCA effects. Positive and significant ĝfi values were observed for number of trusses per plant (1.69), number of fruits per truss (0.42) and mean fruit weight (1.69), while positive and significant ĝmi values were observed for days to fruiting and fruit ripening (0.81 and 0.99 respectively). This underscores the individualistic contributions of each parent variety to specific traits.

The MB variety mirrors the trends observed in CB and MA. Noteworthy differences in magnitudes and directions of ĝfi and ĝmi values underscore the variety-specific nature of parental contributions. Positive and significant ĝfi values (1.58 and 1.65 and 2.23) were observed for days to fruiting, fruit ripening and mean fruit weight respectively, whereas negative ĝmi values were observed for other traits except mean fruit weight with 1.17.

The partitioning into female and male effects provides insights into the specific parent influencing each trait. Traits with strong ĝfi or ĝmi effects, present targeted opportunities for improvement. These insights serve as valuable guidance for breeders, for informed decision-making in breeding programs aimed at achieving specific trait enhancements.

Table 1

GCA effects (ĝ_i), and the adjusted partitioning of the GCA effects to estimate female (ĝ_fi) and male (ĝ_mi) effects of the tested three parents.
Varieties	GCA	Frt	FRp	Truss	F/Trs	MFW	HvtD	ShfL
CB	ĝ_i	-0.18	0.44	-0.51	0.50	-1.58	0.46	0.81
	ĝ_fi	0.37	1.54	-1.28	0.81	-3.93	0.40	1.36
	ĝ_mi	-0.73	-0.66	0.26	0.18	0.77	0.51	0.26
MA	ĝ_i	-0.57	-1.10	1.25	0.41	-0.12	-0.04	-0.02
	ĝ_fi	-1.94	-3.19	1.69	0.42	1.69	-0.04	-0.40
	ĝ_mi	0.81	0.99	0.81	0.40	-1.94	-0.04	0.37
MB	ĝ_i	0.75	0.66	-0.73	-0.18	1.70	-0.42	-0.79
	ĝ_fi	1.58	1.65	-0.40	-0.95	2.23	-0.37	-0.95
	ĝ_mi	-0.08	-0.33	-1.06	-0.59	1.17	-0.48	-0.62
SE	ĝ_i	0.23	0.47	0.28	0.09	0.82	0.26	0.25

Frt = Days to fruiting; FRp = Days to fruit ripening; F/Trs = No of fruits per truss; MFW = Mean fruit weight per plant; HvtD = Harvest duration; ShfL = Shelf life.

Maternal effect

Table 2 shows the adjusted maternal effects of the tested three parents. In plant breeding, understanding maternal effects is pivotal for deciphering the intricate interplay between parent varieties and specific traits. The table presented sheds light on maternal effects across various traits for the three parents.

The maternal effects for the CB variety are distinctive across traits. For days to fruiting and days to fruit ripening, the maternal influence is positive and significant at 0.55 and 1.10, respectively, suggesting that longer durations are associated with the maternal parent. Significant negative effects were observed for truss formation (-0.77) and mean fruit weight (-2.35), indicating that these traits were adversely impacted by the maternal parent.

In the MA variety, significant negative maternal effect was observed for days to fruiting (-1.38) and days to fruit ripening (-2.09), suggesting a shorter time to fruiting and ripening influenced by the maternal parent. Positive and significant effects are evident in traits such as number of trusses (0.44) and mean fruit weight (1.82), implying favorable maternal influence. The maternal effects on number of fruits per truss and harvest duration are neutral, hovering around zero.

The MB variety exhibited unique maternal effects as well. Positive and significant influences are observed for days to fruiting (0.83), days to fruit ripening (0.99), number of truss (0.33) and mean fruit weight (0.53) indicating that these traits benefit from the maternal parent. However, significant negative effects were recorded for number of fruits per truss (-0.18) and shelf life (-0.17). Understanding maternal effects is crucial for making informed decisions in breeding programs. Positive maternal effects in certain varieties for specific traits suggest the potential for targeted trait improvement through careful selection of maternal parents. Data showed that the average of the difference between ĝfi and ĝmi is exactly equal to maternal effect according to Cockerham (1963), which is based on the average of the females over all associated males. This advancement in methodology aligns with studies by Mahgoub (2011) and Fan et al., (2014), emphasizing the importance of refining the estimation of maternal effects for enhanced precision in plant breeding practices.

Table 2

Adjusted maternal effects of the tested five parent.
Varieties	Frt	FRp	Truss	F/Trs	MFW	HvtD	ShfL
	(Days)	(Days)	(Num)	(Num)	(g)	(Days)	(Days)
CB	0.55	1.10	-0.77	0.32	-2.35	-0.06	0.55
MA	-1.38	-2.09	0.44	0.01	1.82	0.00	-0.38
MB	0.83	0.99	0.33	-0.18	0.53	0.06	-0.17
SE	0.13	0.27	0.16	0.05	0.48	0.15	0.14

Frt = Days to fruiting; FRp = Days to fruit ripening; F/Trs = No of fruits per truss; MFW = Mean fruit weight per plant; HvtD = Harvest duration; ShfL = Shelf life.

Specific combining ability

The calculated Specific Combining Ability (SCA) effects, employing Griffing's method and the subsequent partitioning, are detailed in Table 3. Days to fruiting and days to fruit ripening revealed that, the reciprocal cross (MA x CB) had negatively significant and much higher values for SCA effects (-10.22 and − 16.32, respectively) after partitioning, compared with its cross (CB x MA) values (-9.72 and − 13.32, respectively). In contrast, when SCA effects are calculated according to Griffing's method, an assumption of uniformity (-1.10 and − 1.28, respectively) for each cross and its reciprocal is made, lacking the additional information revealed by the partitioning.

Similarly, the cross (CB x MB) had SCA effects with highly significant and much higher values after partitioning (-9.46 and − 2.68), compared with their reciprocals (MB x CB) for mean fruit weight and harvest duration (-0.24 and − 2.35), respectively. Also, cross (MA x MB) had significant and much higher SCA effect values after partitioning for days to fruiting and days to fruit ripening (-10.75 and − 15.71, respectively), compared with their reciprocal (MB x MA) with (-7.08 and − 12.38, respectively). These findings from the partitioning process provide valuable insights beyond the assumptions made by Griffing's method, offering a more detailed understanding of the specific combining abilities within each cross.

Table 3

SCA effects according to Griffing’s method (upper) and SCA effects according to the proposed method (bold, lower) of F₁ crosses (F₁) and their reciprocals (F_1r).
	SCA	Frt	FRp	Truss	F/Trs	MFW	HvtD	ShfL
CB,MA	Griffing's	-1.10	-1.28	1.07	-0.01	0.49	-1.75	0.85
CB x MA	F₁	-9.72	-13.32	-1.26	-0.11	-2.33	-2.26	-0.62
MA x CB	F_1r	-10.22	-16.32	-1.26	-0.78	-4.43	-2.43	-1.79
MA,MB	Griffing's	-0.10	-0.51	-0.61	-0.01	-5.77	-1.86	-0.04
MA x MB	F₁	-10.75	-15.71	-1.37	-0.44	1.11	-2.15	-2.37
MB x MA	F_1r	-7.08	-12.38	-2.70	-1.11	-6.50	-2.32	-2.37
CB,MB	Griffing's	1.13	1.61	-1.05	-0.23	-0.78	-0.53	-1.04
CB x MB	F₁	-8.61	-14.33	-3.64	-1.11	-9.46	-2.68	-1.51
MB x CB	F_1r	-9.77	-14.66	-1.31	-0.44	-0.24	-2.35	-2.01
SE		0.36	0.74	0.44	0.14	1.30	0.41	0.39
Frt = Days to fruiting; FRp = Days to fruit ripening; F/Trs = No of fruits per truss; MFW = Mean fruit weight per plant; HvtD = Harvest duration; ShfL = Shelf life

In this study, a proposed model was used to partition General Combining Ability (GCA) and Specific Combining Ability (SCA) effects, enabling the estimation of these effects for each parent when used as a female or a male in hybrid combinations. The results disclosed valuable insights into the genetic contributions of each parent, shedding light on their roles in specific trait expressions. The estimation of GCA effects using Griffing's method, after partitioning, revealed an interesting symmetry. The calculated GCA effects were found to be equal to the average of GCA effects for each parent when used as both a male and a female in hybrid combinations. This observation highlights the consistency and reliability of the proposed model, providing a robust approach to discerning parental contributions.

Furthermore, the average of the difference between female and male GCA effects emerged as a precise and valid estimator of maternal effects. Specifically, CB and MA exhibited significant negative maternal effect values for mean fruit weight and days to fruiting and fruit ripening, respectively. This underscores the utility of maternal effects in accurately estimating favorable alleles, particularly those with additive characteristics.

The calculation of SCA effects according to Griffing's method yielded an average of SCA effects for each cross and its reciprocal. In contrast, the proposed model introduced in this study demonstrated that the average difference between SCA effects of each cross and its reciprocal is equivalent to the reciprocal effects. This finding refines our understanding of specific combining abilities, offering a nuanced perspective on the interactions between different parental combinations.

In conclusion, the partitioning of GCA and SCA effects according to the proposed model enriches the precision of estimations for each parent's contributions in hybrid combinations. The consistent findings across various traits and parent combinations underscore the reliability and applicability of the introduced model, providing a valuable tool for plant breeders in enhancing their understanding of genetic interactions and optimizing breeding strategies.

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Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

The research was funded by the authors.

Authors' contributions

M.I. conceptualized and designed the study, making substantive revisions to the manuscript. B.B. conducted data acquisition, analysis, and interpretation. All authors reviewed and endorsed the final manuscript.

Acknowledgements

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Plant material information

The tomato (Solanum lycopersicum) plants include a commercial hybrid variety “Cobra” acquired from the Department of Crop Science, University of Nigeria, Nsukka seed bank and two mutants “MA” and “MB” generated in the Department of Crop Science, University of Nigeria, Nsukka, breeding program by Prof. M.I. Uguru, and a voucher specimen was deposited at the Department of Crop Science, University of Nigeria, Nsukka seed bank.

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No competing interests reported.

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Estimating Maternal Effects on Yield Traits in F 1 Hybrids of Tomato (Solanum lycopersicum) Using a Modified Diallel Cross Model

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Abstract

Introduction

Materials and Methods

Genetic Materials and Cross Model

Statistical Analysis

Proposed Model Formula

Results and Discussion

General Combining ability

Maternal effect

Specific combining ability

Conclusion

Declarations

References

Additional Declarations

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