HORTSCIENCE 30(2):325–328. 1995.

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Heritability and Patterns ofInheritance of the Ripening Dateof ApplesStephen J. Tancred and Aldo G. ZeppaDepartment of Primary Industries, Granite Belt Horticultural Research StatP.O. Box 501, Stanthorpe Q4380, Australia

Mark CooperDepartment of Agriculture, The University of Queensland, Brisbane Q4Australia

Joanne K. StringerBureau of Sugar Experimental Stations, P.O Box 86, Indooroopilly Q4Australia

Additional index words. Malus domestica, apple breeding, heritability, combining ability

Abstract. A major objective of the apple (Malus domestica Borkh.) breeding program inStanthorpe, Australia, is to develop early ripening, high-quality cultivars. The heritabilityand inheritance of ripening date was investigated. Regression of offspring on midparentharvest dates and estimation of best linear unbiased predictions for parents were used demonstrate that apple harvest date is highly heritable. Predominantly, additive geneticcomponents of variance are responsible for the variation. Despite the existence of somespecific combining ability variance and some non-normal family distributions, the beststrategy for a breeder to predict the harvest date of progeny is to calculate the mean harvedate of parents.

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Table 1. Ripening date of 13 apple cultivars used asparents at Stanthorpe, Australia. Ripening dateexpressed as day relative to ‘Jonathan’.

Parental cultivar Ripening dateStark’s Earliest –45Milton –43Early McIntosh –37Canterbury –36

Apple breeding is a long-term and costprocess due to the long juvenility period athe large size of mature apple trees. However,because apples are vegetatively propagateselected cultivar is genetically fixed and chave industry use for hundreds of years (Brow1975).

Stanthorpe is Australia’s earliest apple prduction district, and a breeding program winitiated to enhance this market advantaThe Queensland Dept. of Primary Industribegan apple breeding at Stanthorpe in 196produce new red dessert cultivars that matubefore ‘Jonathan’, the standard early cultivand that were of a higher quality than tcommercially available early cultivars. Be-cause the eating quality of early season appis often inferior to that of mid- and late-seasapples, the breeding plan had the two paraobjectives of earliness and high eating qualThree cultivars that mature before ‘Jonathahave been released from the Stanthorpe pgram: ‘Earlidel’, ‘Summerdel’, and ‘GB 6343’ (Tancred et al., 1994).

Because quantitative studies of fruit genics have usually been done retrospectivfrom breeding program data, they often lacspecific design for estimation of heritability

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Received for publication 12 July 1994. Accepted forpublication 7 Dec. 1995. We thank Susan K. Browfor reviewing the manuscript and Halina Kruger andChandra Smith for their help with data entry. Thecost of publishing this paper was defrayed in part the payment of page charges. Under postal regutions, this paper therefore must be hereby markadvertisement solely to indicate this fact.

Ruby Gem –34Carrington Red –33William’s Favourite –30Earliblaze –26Jonathan 0Sayers 7Delicious 10Golden Delicious 22Granny Smith 47

This, too, is the case for the Stanthorpe gram. However, genetic parameters have busefully estimated in this manner for sevetree fruit crops (Abe et al., 1993; Dicenta et1993; Hansche et al., 1966, 1972a, 197Thompson and Baker, 1993), and we adosimilar strategy.

Only a few studies have been madeapple ripening date, and they all concludeshowed polygenetic inheritance. Crane andLawrence (1933) observed that no shadiscontinuous variation occurred and thatmajority of progeny ripened between the pents. Howlett and Gourley (1946), Bisho(1951), and Davis et al. (1954) concurred wthis finding, but Hartman and Howlett (194found transgressive segregation with a conerable percentage of progenies earlier thaearly parent and some later than the late paBrown (1960) found the progeny mean average 2 weeks earlier than the midparevalue, except for crosses involving very lparents, where the progeny mean was upmonths earlier than the midparent mean. Brown(1975) reviewed the breeding and geneticapples and Brown (1992) has reviewed inheritance of Mendelian traits in apples. Wayet al. (1990) have described Malus spp. ge-netic diversity.

Breeders at Stanthorpe hoped that bybridizing early ripening parents with higfruit-quality parents, families would be genated that had a sufficient number of seedlthat matured before ‘Jonathan’, to enablelection to be made within these on fruit quacharacters. This study reports the variatioripening date within and among families p

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duced in the Stanthorpe apple breeding pgram. Several quantitative methods that be used as predictive selection tools are uFruit quality data will not be discussed her

Materials and Methods

Parent cultivars and hybridizations. Bipa-rental hybridizations were done among early, mid-, or late-maturing apple cultivafrom 1964 to 1970. The parents were selectefrom the best available in Australia at the tim(Table 1). Two of the cultivars are full-sib(‘Milton’ and ‘Early McIntosh’), but no ge-netic relationship is known to exist betweany of the others. Thirty-six families wereproduced with an average size of 286 invidual trees (range 16 to 1100). The seedlingswere field-planted between 1966 and 19Only two sets of reciprocal crosses were mad‘Milton’ x ‘Early McIntosh’ and ‘Golden Delicious’ x ‘Jonathan’.

Planting design. Because the primary aimwas to select suitable cultivars for commercuse, there was no planned trial layout or recation for the purposes of this study. Treeswithin a family were planted beside each otin orchard rows each year. However, becausseveral crosses were made over a numbeyears, complete families were not alwaplanted together.

Population management. Seedlings wereevaluated for ripening date every 2 to 5 daduring the harvest period. Ripening date wasdetermined by subjective assessment of ftexture, flavor, blush color, and backgroucolor. Seedlings were culled or further propgated after several years of consistent permance. Seedling trees were observed croping for 3 years, on average. About 16% of theseedlings planted never cropped and weredisregarded in all calculations. Observationswere made from 1973 to 1985, when torchard was removed.

Seasonal adjustments. Due to weathervariation between years, the harvest dateany particular genotype may vary from yearyear. These year effects were considered tofixed effects in the analyses. To account forthese effects, each year was assigned an eness or lateness factor from the harvest dof standard cultivars on the research staand on district farms. This factor ranged from

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Fig. 2. Offspring midparent regressions of ripening date for 36 apple families. Ripening date expressed asdays relative to ‘Jonathan’. Regression equation: y = 0.94x – 2.4.

Fig. 1. Frequency distributions of ripening date in four families of apple seedlings: (A) ‘William’s Favourite’x ‘Early McIntosh’, (B) ‘William’s Favourite’ x ‘Golden Delicious’, (C) ‘Delicious’ x ‘Granny Smith’,and (D) ‘Milton’ x ‘Carrington Red’. Only families (A) and (B) have normal distributions. Arrowsindicate parent cultivar ripening dates. Ripening date expressed as days relative to ‘Jonathan’.

14 days early to 14 days late. For the 13 yearsof observation, it averaged 1.3 days earHarvest dates of individual progeny withifamilies were adjusted by this factor for eayear. Harvest dates for each tree were thaveraged across years. All harvest dates areexpressed relative to that of ‘Jonathan’.

Genetic analysis. The parents used spannea wide range of maturity periods (Table 1) awere considered to constitute a random samfrom the base population accessed by Stanthorpe breeding program. Narrow-senseheritability (h2) was estimated using the linearegression of year-adjusted offspring perfomance on the average performance of thparents, or midparent value (Falconer, 198Three procedures for estimating offsprinmidparent regression were investigated folowing Kempthorne and Tandon (1953) anBohern et al. (1961): 1) the regression of tphenotypic mean of all offspring from a givebiparental combination on the midparent valu2) the regression of offspring on midparent,which the midparent values were repeated each of the progeny; and 3) the weightregression technique of Kempthorne aTandon (1953). As have been found by othersthe results of each procedure were similar, aonly the first procedure, the regression of tphenotypic mean of all offspring on thmidparent value, is presented.

The assumption that the effects of enviroment are randomly distributed among the indviduals, so that the environmental correlatiobetween individuals in a progeny group is ze(Bohern et al., 1961), is unlikely to be fulfilledHowever, since all progeny from a cross wenot grown adjacent to each other, there is soprotection against such environmental corrlations. Nevertheless, any environmental corelations that do exist may increase the coriance among family members. Therefore,estimates of genetic parameters should treated with some degree of care.

General combining ability (GCA) effectsof the parents and specific combining abili(SCA) effects for all biparental combinationwere obtained by applying the method of belinear unbiased prediction (BLUP). The mat-ing design model is an incomplete diallel without reciprocals where:

Yijk = µ + gj + gk + sjk + eijk andYijk is the phenotypic observation for the ithprogeny member of the family jk;µ is the population mean;gj is the random variable associated with tGCA of the jth female;gk is the random variable associated with tGCA of the kth male;sjk is the random variable associated with tSCA of the parents j and k;eijk is the random error associated with the ithprogeny member of the family jk.

Analyses were performed usinGiesbrecht’s algorithm of restricted maximulikelihood (Huber, 1993). The BLUP theorywas developed specifically to analyze diverand unbalanced performance data from dacattle (Henderson, 1963, 1973, 1977a, 1977The BLUP theory has successfully beeadapted to predict future performance of pa

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ents in forest tree breeding (White and Hod1988). Forest tree breeding shares many of experimental design problems found in apbreeding. The Wilk–Shapiro test was undetaken to test the normality of the data for eafamily (Proc. Univariate; SAS, 1990).

Results and Discussion

All the individual families showed continuous distribution around the midparent w

no evidence of segregation due to major geneffects. Thirteen of the 36 families had non-normal distributions, either due to excessivskewness or kurtosis. Examples of two normaland non-normally distributed families areshown in Fig. 1.

The mean harvest date of all progeny wa–10.2 days, which was only 0.6 days earliethan the mean (weighted) of all midparentsOn a family basis, the mean of the 36 familiewas –13.4 days, which was only 0.9 days

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Table 2. General combining ability (GCA) for rip-ening date of 13 apple cultivars used as parents.

Parental cultivar GCAz

Stark’s Earliest –16.13Milton –11.67Early McIntosh –9.27Canterbury –12.96Ruby Gem –0.21Carrington Red –6.69William’s Favourite –9.62Stark Earliblaze –11.00Jonathan 8.29Sayers 3.98Delicious 13.83Golden Delicious 14.66Granny Smith 36.78zGCA expressed as ripening date relative to‘Jonathan’.

Table 3. Specific combining abilities (SCA) of 36apple crosses for ripening date. Ripening dateexpressed as days relative to ‘Jonathan’.

Cross SCAz

Milton x Early McIntosh –5.70Milton x Ruby Gem –2.81Milton x Carrington Red 1.48Milton x Williams Favourite 1.62Early McIntosh x Milton –0.16Early McIntosh x Carrington Red 0.07Early McIntosh x Sayers 7.22William’s Favourite x Early McIntosh –3.08William’s Favourite x Sayers –3.31William’s Favourite x Golden Delicious 5.56Jonathan x Stark’s Earliest 4.21Jonathan x Milton 1.47Jonathan x Early McIntosh 1.61Jonathan x Canterbury 3.72Jonathan x Ruby Gem 3.12Jonathan x Carrington Red 0.99Jonathan x Stark Earliblaze –10.85Jonathan x Sayers –2.24Jonathan x Golden Delicious –1.59Delicious x Stark’s Earliest –5.93Delicious x Milton 2.85Delicious x Early McIntosh –1.28Delicious x Canterbury –5.10Delicious x Ruby Gem –0.36Delicious x Carrington Red 0.23Delicious x William’s Favourite –1.83Delicious x Stark Earliblaze 9.68Delicious x Jonathan 2.41Delicious x Sayers –1.57Delicious x Golden Delicious 0.67Delicious x Granny Smith 1.69Golden Delicious x Early McIntosh –1.59Golden Delicious x Carrington Red –1.51Golden Delicious x Jonathan 0.02Granny Smith x Early McIntosh 1.92Granny Smith x Sayers 0.32zSCA expressed as ripening date relative to‘Jonathan’.

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earlier than the average midparent harvdate. These average harvest dates are oslightly earlier than the midparent dates, whicontrasts with the 2 weeks earlier reportedBrown (1960). The sample variation of alprogeny was 438.7, and of all midparenaccounting for family size, it was 175.3.

Brown (1960) found that families from twlate-ripening parents produced only a smproportion of their progeny as late ripeningphenomenon we did not observe, possibecause only a few of these types of croswere made in the Stanthorpe program. Brown(1975) proposed a minimum ripening date thawas fixed by a minimum fruit developmenperiod after bloom. He used this relationshipto explain why crosses between two earipening parents would produce a populatiskewed toward lateness and with reduced vation. This result was absent with our earlyxearly families, possibly because this theorecal limit of earliness was not yet reached.

Narrow-sense heritability (h2) for harvestdate was 0.94 ± 0.067 (Fig. 2), a relatively highvalue for a quantitative character, but constent with the high estimates found for harvedate of Japanese pear (Pyrus pyrifolia Nakai)(Abe et al., 1993), sweet cherry (Prunus aviumL.) (Hansche et al., 1966; Hansche and Broo1965), peach (Prunus persica L. Batsch)(Hansche et al., 1972b), and walnut (Juglansregia L.) (Hansche et al., 1972a). Regressionof Brown’s (1960) apple cultivar progenmeans on midparent values reveals that, indata set, h2 was 0.69 ± 0.071.

Heritability, as we have measured it, canoverestimated if basic assumptions are vlated. These commonly include the existenof dominance or epistatic genetic componeor prior inbreeding within the parents (Faconer, 1989; Fernandez and Miller, 198The former is assumed to be low and the lais known to be negligible amongst our parenIf significant genotype × environment (G × E)interaction exists, then maturity re-rankinwill occur in different environments and yearIgnoring this G × E interaction will also causeh2 to be overestimated. This hazard can avoided by growing parents and offspring different environments (Casler, 198Fernandez and Miller, 1985). This was thecase in our experiments, where the parewere grown in a repository under better horcultural conditions than the progeny. Also, theyear effects on progeny were reduced by justing for season, then averaging across yeAlternatively, if the variation differs betweeparents and offspring, then the regression be done on standardized data ( Frey and Hor1957). This procedure gave an estimate heritability of 0.924 ± 0.065, which is notdifferent from that based on the year-adjusdata.

The high narrow-sense heritability we foundfor harvest date implies that additive geeffects are predominantly controlling inherance. This finding is supported by the BLUanalysis where the variance componentGCA (237.8) was nearly 10 times the variancomponent of SCA (25.4). The GCA esti-mates (Table 2) can be used to predict

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progeny mean of future crosses within tparental set. The rank order of parent ripenindate and parent GCA is similar when these tvariables are regressed, r2 = 0.91.

The SCA effects of each cross (Tableindicate deviations from the expected progemeans as predicted by GCA. They have no useoutside of the actual crosses from which thwere measured, but their small size in relatto GCA effects supports the strong influenof additive genetic effects on the inheritanof maturity.

A knowledge of heritability and combining ability estimates can be useful when planing crosses for a specific ripening periodcan also be used to predict average ripendates of crosses made for other objectivDespite variable distributions within familiethe best strategy for producing a populationearly maturing apple seedlings is to crocultivars that have an early midparent ripendate. A knowledge of the inheritance of fruquality characteristics can then be appliedpredict the range of fruit quality that will exiswithin families.

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