Journal of Heredity Advance Access published online on September 23, 2008
Journal of Heredity, doi:10.1093/jhered/esn075
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On the Genetic Control of Heterosis for Fruit Shape in Melon (Cucumis Melo L.)
From the Departament de Genètica Vegetal, IRTA, Centre de Recerca en Agrigenómica (CSIC-IRTA-UAB), Ctra de Cabrils, Km 2, E-08348 Cabrils, Spain (Fernández-Silva, Moreno, Eduardo, Arús, and Monforte); and the Centro de Investigación y Tecnología Agroalimentaria de Aragón, Centro de Investigación y Tecnología Agroalimentaria de Aragón, Apartado 727, 50080 Zaragoza, Spain (Álvarez)
Address correspondence to A. J. Monforte at the address above, or e-mail: antonio.monforte{at}irta.es.
The objective of the present work is to study the genetic basis of heterosis for fruit shape (FS) in melon observed in a cross between the Spanish cultivar "Piel de Sapo" (PS) and the Korean accession PI 161375 (Songwang Charmi [SC]) using a set of near-isogenic lines (NILs) with contrasting phenotypes for FS, each carrying a single chromosomal introgression from SC within the genetic background of PS. We investigated the FS of homozygous NILs, hybrids NIL x PS, and all 2-way crosses between NILs to test the main heterosis hypotheses (dominance, overdominance, and epistatic interactions). Gene action of alleles of quantitative trait loci inducing fruit enlargement was dominance, whereas those inducing rounder fruit were additive or recessive. Only minor epistatic interactions were found. Therefore, the most plausible explanation for FS heterosis in this cross is in agreement with the dominance complementation hypothesis. Over 70% of the hybrid heterosis could be achieved by combining just 2 loci, indicating that the genetic control of FS heterosis in this cross is relatively simple. FS is proposed as a reproductive trait in melon because of the high correlation to the number of seeds produced along the fruit longitudinal axis.
Heterosis or hybrid vigor refers to the phenomenon by which an F1 hybrid exhibits phenotypic characteristics superior to the mean of the 2 parents (midparent heterosis) or to either of them (best-parent heterosis). Heterosis is a widely documented feature of diploid organisms that undergo sexual reproduction in both the animal and plant kingdoms, described in the early work of Schull (1908) and East (1936). Heterosis and inbreeding depression are considered 2 aspects of the same phenomenon, with the superior phenotype of the hybrid being lost during inbreeding but recovered by outcrossing (Falconer and Mackay 1996). The phenomenon has been exploited extensively in agriculture; the cultivation of hybrid varieties has had a major role in the improvement of crop production over the past few years (Duvick 1999). Heterosis also has an important role in the fitness of natural populations. Correlation between fitness and heterozygosity in natural populations has been extensively documented (Hansson and Westerberg 2002). Inbreeding depression may contribute to the formation of reproductive barriers between species and populations, whereas heterosis may be important in maintenance of genetic variation in populations (Crow 1986).
The genetic basis of heterosis has been discussed since the early works, but we are still far from a definitive answer (see recent reviews: Birchler et al. 2003; Lippman and Zamir 2007; Springer and Stupar 2007). Interest in heterosis research has been revitalized with the new advances in genome sequencing (Fu and Dooner 2002) and gene expression analysis (Guo et al. 2004, 2006). Several hypotheses have been proposed. The dominance complementation model proposes that the enhanced phenotype of the hybrids is the result of complementation of deleterious recessive alleles present in each inbred parent that are masked by dominant alleles in the F1 hybrid (Bruce 1910). The second hypothesis is the true overdominance model, where a heterozygous combination of alleles at a single locus is superior to a homozygous combination (East 1936; Crow 1948). Overdominance can also be explained by pseudo-overdominance, which is a case of dominance complementation in which the 2 recessive mutations are linked in repulsion. The third hypothesis is epistasis, that is, gene-by-gene multiplicative interactions (Allard 1996). The genetic basis of heterosis may also depend on the trait or cross, being one of the above hypotheses the major cause in a particular case, although an alternative hypothesis may be more important in another cases. In addition to the genetic complexity underlying heterosis, most of its associated traits, such as yield, are themselves under complex genetic control, strongly influenced by environmental conditions and with low heritability, making their genetic analysis even more difficult.
Quantitative trait locus (QTL) mapping in rice, maize, and other organisms have addressed the classical models by breaking down heterosis into Mendelian factors and assessing modes of inheritance (Stuber et al. 1992; Xiao et al. 1995; Yu et al. 1997; Monforte and Tanksley 2000; Li et al. 2001; Luo et al. 2001; Steinmetz et al. 2002; Hua et al. 2003). The results indicate that both dominance and overdominance have an important role in heterosis. The role of epistasis is variable, being important in some experiments (Monforte and Tanksley 2000; Li et al. 2001) but having little effect in others (Stuber et al. 1992; Xiao et al. 1995). One important result from the research is that heterosis can be defined by a limited number of genetic factors, so they can be studied by QTL analysis, opening up the possibility of cloning QTLs involved in heterosis.
Best-parent heterosis for fruit shape (FS) is common in melon (Cucumis melo L.), especially in hybrids between exotic accessions and the "inodorous"-type cultivar "Piel de Sapo" (PS) due mainly to the longitudinal enlargement of the fruit (Monforte et al. 2005). Melon FS is a polygenic and highly heritable trait; several major QTLs with consistent effects in different experiments have been described (Périn et al. 2002; Monforte et al. 2004; Eduardo et al. 2007). This makes melon FS a suitable system for dissecting the genetic and molecular basis of heterosis.
The F1 hybrid from the cross between the Korean accession PI 161375 "Songwang Charmi" (SC) and PS cultivar shows a strong best-parent heterosis for FS, being 45% more elongated than any of the parents, which fruit showed a similar length:diameter. The later result has been extensively documented across a variety of trials in different years, field locations, and experimental conditions (Monforte et al. 2004, 2005). The objective of this work was to study the genetic basis of the heterosis for FS in this cross. We used a set of near-isogenic lines (NILs) recently developed (Eduardo et al. 2005) each carrying a single introgression fragment derived from SC within the genetic background of PS. NILs are devoid of whole-genome epistatic interactions, so direct hypothesis for dominance effects at a single locus and controlled epistasis experiments can be carried out (Eshed and Zamir 1996; Monforte et al. 2001; Semel et al. 2006). We investigated the progeny of various crosses between NILs with contrasting phenotypes for FS and the PS parent to estimate the gene action mode at the single QTL level and all possible reciprocal crosses between these NILs to estimate 2-way dominant x dominant epistatic interactions at these QTLs. Based on the results obtained, we discuss which of the 3 major heterosis hypotheses (dominance, overdominance, or epistasis) may explain the genetic basis of FS heterosis in melon.
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Plant Material
The melon PS inodorous-type cultivar and the exotic Korean accession SC (PI 161375) were the parent genotypes. Four NILs, sharing the genetic background of the PS and each with a unique SC introgression (Eduardo et al. 2005) harboring previously identified major FS QTLs, were selected: SC8-3 and SC10-2 produce elongated melons and SC12-1 and SC6-4 round ones (Eduardo et al. 2007). Due to the isogenic nature of these genotypes, differences among them and the recurrent genotypes PS can be attributed to a unique QTL included in their respective introgression from SC. The introgressions of SC6-4, SC8-3, SC10-2, and SC12-1 are located in linkage groups VI, VIII, X, and XII, respectively (Eduardo et al. 2005). These NILs were backcrossed to PS, resulting in 4 hybrid genotypes carrying a single-dose introgression (NILF1). All possible 2-way crosses between these 4 NILs were done to obtain hybrid lines carrying 2 different single-dose introgressions (NIL1 x NIL2). The genotype of each cross was verified using molecular markers defining the target introgression according to Eduardo et al. (2005).
Field Experiments
A preliminary experiment (Cabrils03) was performed during the summer of 2003 in Cabrils (Spain). Ten plants of PS, SC10-2, and SC10-2F1 were randomly distributed in a greenhouse and grown in drip-irrigated peat bags, with 0.25 m spacing between plants. The 2 major experiments, including all the NILs, and NIL1 x NIL2 crosses were performed during the summer of 2005 in Cabrils and Zaragoza (Spain), designated as Cabrils05 and Zaragoza trials. In Cabrils, plants were grown as in 2003. The greenhouse was divided in 4 blocks. In all, 4 plants of each NILF1 and NIL1 x NIL2 crosses, 4 of PS, and 2 of each SC, F1 (the hybrid between PS and SC), and homozygous original NILs were randomized within each block. Plants were hand pollinated, allowing only one fruit per plant. In Zaragoza, plants were distributed in plots of 3 plants. In total, 10 plots of PS, 4 plots of SC, F1, and each homozygous NIL, and 8 plots of each NILF1 and NIL1 x NIL2 crosses were randomized in the field. The flowers were open pollinated; and 1–8 fruits were harvested from each plot.
SC12-1, SC12-1F1, and PS were re-evaluated in Cabrils during 2007 in the greenhouse (Cabrils07g) and field (Cabrils07f). In both cases, 10 plants of each were completely randomized in the greenhouse or field, respectively, following the same horticultural cultures explained above.
The agronomic evaluation included the following traits: fruit weight (FW) in grams, fruit length (FL) in centimeters, maximum fruit diameter (FD) in centimeters, FS as the ratio FL/FD, corresponding to FS I defined by Brewer et al. (2006), and soluble solid concentration (SSC) measured from melon flesh crude extract as °Brix with a hand refractometer. The number of seeds on the fruit vertical axis (SN) was counted from digital photos of longitudinally opened fruit obtained only in the Cabrils05 trial. Seeds were not clearly visible in every fruit, producing a reduction in the number of replicates in some cases.
Data Analysis
All statistical analyses were performed with JMP 5.1.2. for Windows (SAS Institute, Cary, NC). Genotypes with less than 4 replicates were not used for analysis. Midparental heterosis of the F1 was tested by the contrast 2F1–PS–SC at P < 0.05, where F1 was the mean of the F1 hybrid and PS and SC the means of the parental genotypes. The gene action mode at single QTLs was tested by the contrast 2NILF1–NIL–PS at P < 0.05, where NIL, PS, and NILF1 were the means of each NIL, PS, and their respective NILF1. The dominance/additive ratio was calculated as d/|a| = (NILF1 – (PS + NIL)/2)/|(PS – NIL)/2|, with |a| being the absolute value of a. Positive values of d/|a| indicate that the value of the hybrid is higher than expected and negative values that is lower than expected, independent of the direction of the additive effect.
Epistatic digenic interactions were studied in Cabrils05 and Zaragoza05 based on the following model of analysis of variance (ANOVA) for each pair of NILs:
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, and 
, the effect of the SC introgressions (fixed effect); Lk, the location effect (Cabrils or Zaragoza [random effect]); 
, the interaction between introgression effects; NIL1Lik + NIL2Ljk, the interaction of each introgression with the locations; NIL1NIL2Lijk, the triple interaction; and eijk, the error or random residual effect. Significance of the effects was studied by an F-test. Epistatic interactions at each location were also tested using the same ANOVA model (removing the location effect) and by the NIL1 x NIL2 + PS – NIL1F1 – NIL2F1 contrast, where NIL1 x NIL2 was the mean of the cross NIL1 x NIL2, NIL1F1 and NIL2F1 the means of the respective NILF1s, and PS the mean of the control PS. When the epistasis contrast was significant, the magnitude of epistasis was calculated as the deviation from the expected value of the double heterozygous as follows:
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NILs carrying a single chromosome segment derived from a donor genotype (usually nonadapted germplasm) on an elite genomic background are suited to study genetic interactions at single QTL level (Monforte et al. 2001; Semel et al. 2006). It is assumed that each introgression represents a unique QTL; however, it is possible that the introgression contains several QTLs affecting the trait under study (Monforte et al. 2001). The genotype of the NIL is estimated with markers distributed through the genome. Depending on marker coverage, small additional introgressions not be detected with the markers may exist (see, e.g., van der Hoeven et al. 2000). Thus, the molecular marker map used by Eduardo et al. (2005) to characterize the melon NIL population had a few gaps larger than 30 cM, so we cannot rule out the possibility that some of the NILs may carry an additional introgression. In order to simplify the interpretation of the results, we will assume that each NIL carries a single QTL.
Table 1 shows the means and standard deviations of the studied traits in parent lines PS and SC and their F1 hybrid. PS fruit from both Cabrils and Zaragoza were large, oval, and with high SSC. In Zaragoza, SC fruit were smaller and slightly pear shaped, with medium SSC content. SC fruit in Cabrils were also smaller and pear shaped (Figure 1), but measurements were not taken as this genotype is sensitive to sulfur dusting, used in the greenhouse to control powdery mildew, which causes necrosis and hinders SC fruit growth (Perchepied et al. 2004; Eduardo et al. 2007). These phenotypes were similar to those observed previously (Périn et al. 2002; Monforte et al. 2004, 2005). The F1 showed significant heterosis for FL, FS, and SSC in Zaragoza.
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Although data from SC were not available in Cabrils, the F1 hybrid showed an extremely elongated fruit in both locations, observed in Figure 1, confirming heterosis for FS described previously (Monforte et al. 2005).
Figure 2 depicts the mean values of NILs and NIL–F1s for the studied traits in all trials (see Supplementary Table 1 for further details). SC8-3 fruit were more elongated than those of PS mainly due to an increase in FL and with higher seed number (SN). Similarly, the SC10-2 fruit were elongated, although the effect was not as strong as in SC8-3. Not enough data points for SN could be obtained for this NIL. SC6-4 fruit were round, with smaller FL and SN and larger FD. We could not obtain enough data for SC12-1 in 2005 because the yield of this NIL was too low. The Cabrils07g and Cabrils07f experiments confirmed that SC12-1 fruit were round with a significant reduction of FL. Effects on FW and SSC were not as consistent as FS across locations. In general, these results agree with those previously published (Eduardo et al. 2007), and they confirm the high heritability of QTLs involved in FS.
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The mode of gene action for the QTL alleles producing more elongated fruit was partially dominant for SC8-3 and completely dominant or overdominant for SC10-2 (Figure 2), similar to SN (the SC10-2 x PS SN mean was significantly different from PS, P < 0.05). In contrast, the mode of gene action of the round allele for FS was additive in SC6-4 and recessive in SC12-1. Interestingly, QTL alleles producing more elongated fruit showed different levels of dominance and QTL alleles producing rounder fruit were additive or recessive. The d/|a| values for FS were always positive, indicating that alleles promoting fruit elongation are in general dominant over alleles reducing elongation. Overdominant gene action was not the most common gene action in any case.
Two-way ANOVA revealed that epistasis was not common among the QTLs studied (Table 2). Only the crosses SC12-1 x SC8-3 and SC6-4 x SC8-3 consistently showed a low degree of negative epistasis for FS. Neither positive epistasis nor multiplicative interactions were observed for FS, suggesting that epistasis has a minor role in heterosis for FS in this cross, if any. In the current report, we have focused on studying interaction among a few QTLs with major effects on the phenotypes, so we cannot discard that epistatic interaction among other QTLs with major effects or those without major effects could be important (Carlborg and Haley 2004).
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Fruit of the double-hybrid NIL SC8-3 x SC10-2 increased the mean FS index by 0.66–0.46 (Cabrils-Zaragoza) more than PS (Figure 3, Supplementary Table 1), that is, 73–72% of the difference in FS between PS and the heterotic F1 hybrid. This corresponds to the sum of the effects of the 2 QTLs without epistatic interactions: SC8-3F1 increased the mean FS by 0.45–0.31 and SC10-2F1 by 0.17–0.13 (Figure 3). This means that the 2 dominant QTLs, without epistatic interaction, produced most of the increment in FS observed in the F1. The difference between SC8-3 x SC10-2 and F1 (0.25–0.18) is within the range of the effects of a single QTL. So it is possible that most of the heterotic F1 phenotype could be recovered just by pyramiding a third QTL with dominant effects. These results demonstrate that much of the heterosis for FS in the F1 hybrid may be explained by dominance at few QTLs, supporting the dominance complementation as the most plausible hypothesis for the observed heterosis in this cross, in contrast to previous studies suggesting that 2-locus or higher order epistasis (Li et al. 1997, 2001; Yu et al. 1997; Monforte and Tanksley 2000; Hua et al. 2002, 2003) and/or overdominance (Stuber et al. 1992; Xiao et al. 1995; Lu et al. 2003; Semel et al. 2006) have an important role in the genetic basis of heterosis. Our results are more similar to those of Ku et al. (1999) in tomato, where 2 FS QTLs act independently to produce elongated fruit.
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Numerous studies report correlation between fitness or reproductive traits and heterozygosity (Hansson and Westerberg 2002; Ferreira and Amos 2006; Lippman and Zamir 2007), indicating that heterosis may have an important role in evolution, maintenance of genetic variability by balancing selection, and domestication. Melon seeds are located within the fruit along the longitudinal axis, such that the more elongated the fruit the higher the number of seeds. There is a resemblance between the location of melon seeds within the fruit and that of kernels on the corncob. Elongated corncobs yield more kernels, being a fitness, reproductive, and agronomic trait and a typical example of heterosis exploited by humans in agriculture (Springer and Stupar 2007). We found a strong correlation between SN and FS (r = 0.96, P < 0.0001) and SN and FL (r = 0.88, P < 0.0001). The mode of gene action is also similar for these traits (dominant for larger FS, FL, and SN and additive/recessive for reduced FS, FL, and SN). Thus, FS in melon can be also defined as a reproductive trait. This hypothesis also agrees with the observation that most traditional and exotic melon varieties, where there is more diversity (mainly Africa and India), are oval or elongated (Stepansky et al. 1999; Monforte et al. 2005; Dhillon et al. 2007).
Heterosis and dominance at single QTLs for elongation is not so common in tomato (Solanum lycopersicum), a model species for fleshy fruit development. FS heterosis is quite variable, from positive heterosis (YongFei et al. 1998; Premalakshmi et al. 2002; Joshi and Kohli 2006) to negative (Kurian et al. 2001) or no heterosis (Rao and Choudhary 1981; Joshi and Kohli 2006). A large number of QTLs involved in final FS have been described (Grandillo et al. 1999; Ku et al. 1999; Lippman and Tanksley 2001; Monforte et al. 2001; van der Knaap and Tanksley 2001, 2003; van der Knaap et al. 2002; Tanksley 2004; Brewer et al. 2007). The mode of gene action for elongation of these loci is also quite diverse. For example, the Solanum pimpinellifolium allele of fs11.1, which induces an increase in FS index in a S. pimpinellifolium x S. lycopersicum var. Giant Heirloom population, is dominant over the round S. lycopersicum allele (Lippman and Tanksley 2001), whereas the allele promoting fruit elongation of "ovate" is recessive or additive with respect to the allele decreasing elongation, depending on the genetic background (Ku et al. 1999). Moreover, van der Knaap et al. (2002) found both dominant and partially recessive gene action for elongation at several QTLs within one experiment.
More melon FS QTLs need to be investigated to assess whether the relationship between fruit elongation and dominance is as common as we found it to be. If it was confirmed, melon FS could be defined as another example of reproductive trait where dominant gene action at QTL level would be common, as found by Semel et al. (2006) for a number of reproductive traits in tomato.
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Supplementary Table 1 can be found at http://www.jhered.oxfordjournals.org/.
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The Spanish Ministry of Education and Science and Fondo Europeo de Desarrollo Regional (European Union, grants AGL2003-09175-C02-01 and AGL2006-12780-C02-01); Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (to I.F.-S.); the Spanish Ministry of Education and Science (to I.E.); the Generalitat de Catalunya (E.M.).
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Acknowledgments |
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We thank Angel Montejo, Antonio Ortigosa, and Fuensanta García for technical support. The authors declare no conflict of interest
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Footnotes |
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Corresponding Editor: John Burke
Received March 28, 2008
Revised July 10, 2008
Accepted August 18, 2008
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