Euphytica 14 (1965):
ON THE INHERITANCE OF THE JUVENILE PERIOD IN APPLE
Institute of Horticultural Plant Breeding, Wageningen
With 2 figures
Received 5 Jan. 1965
The following observations were made on the inheritance of the juvenile period (elapsing between seed germination and first flowering) of apple seedlings.
1. Highly significant correlations (0.52 and 0.78 at n = 382 and 71) were found between the length of the juvenile period and the degree to which seedlings or progenies as a whole show juvenile symptoms. This relation may provide a basis for the early elimination of seedlings with a relatively long juvenile period (and which are possibly late-bearing).
2. Significant correlations (ca. 0.5 at n = 42-80) existed between the length of the juvenile period of progenies and parent characters such as season of flowering, season of fruit picking (ripening) and the length of the growth period of the fruits (elapsing between flowering and picking). It is suggested that these characters are measures of the (fruit) growth rate and as such influence the juvenile period of the progenies.
3. A strong correlation (0.77 at n = 42) existed between the length of the juvenile period of the progenies and the length of the vegetative period of the parents (period elapsing between grafting and first-bearing). This infers that seedlings of late-bearing parents would inherit two undesirable characters as they would probably come late into bearing both in the juvenile and the adult phase.
4. Presumptive evidence suggested that the factors which govern flowering in the juvenile and the adult phase are the same in both instances.
The juvenile phase of woody plants is a phenomenon which has intrigued the plant physiologist and handicapped the plant breeder. Numerous studies made by research workers of both categories have considerably contributed to the knowledge about it, they have e.g. disclosed that the (juvenile) period between seed germination and first flowering can generally be shortened by providing optimal conditions for growth or (for apple) by grafting on a precocious rootstock (see also VISSER, 1964), which observations are of practical value to the plant breeder. Surprisingly, as far as the author knows, no investigations have been carried out in the domain of the plant breeder, e.g. as to how the juvenile period is inherited, specifically as regards to what characters, recognizable in the parents, it is genetically related. Such knowledge could be of assistance in shortening the juvenile period by breeding and selection.
Apart from a tentative suggestion made by KARNATZ (1963) regarding the early selection of seedlings as to their prospective juvenile period on the basis of leaf characters, the information about this subject seems to be equally scant.
With the above in mind it seemed useful to relate some observations on the inheritance of the juvenile period in connection with both parent and seedling characters.
Use was made of seedling material obtained from a great number of crosses made among commercial apple varieties between 1950 and 1956. These seedlings, following germination in flats, were usually kept for at least two years in the nursery of the Institute of Horticultural Plant Breeding at Wageningen. Afterwards they were transplanted into the Experimental garden at Elst at distances of 2-2.5 m in the row and of 4-4.5 m between rows. On the whole the seedling areas were treated as a commercial orchard with regard to manuring and other cultural treatments. Pruning was generally light and restricted to the minimum required to shape the tree to some extent and to provide "light and air".
As to the terms employed in this paper, the term "juvenile phase" is only used when it refers to the phase of development through which the seedling passes before it is "adult", e.g. as may appear from the changes in certain morphological characters. The term "juvenile period" refers specifically to the period in years which elapses between the time of seed germination and the first time that the seedling flowers. The term "vegetative period" is only used with reference to the period which elapses before an "adult" cultivated variety comes into bearing following budding or grafting on a rootstock.
3.1. Juvenile period and degree of juvenility
Seedlings in their juvenile phase generally show a number of anatomical and morphological characters which disappear or change with time. For example, according to FRITSCHE (1948), MURAWSKI (1957), KARNATZ (1963) and others the leaves of a juvenile seedling differ from those in the adult phase as to size (smaller), width (narrower), serrations (sharper), cell size (larger), etc. Besides these differences in leaf characters, one of the visually most notable symptoms of "juvenility" is the presence of thorns and initially also the wide angle between side shoots and main stem. On the whole the absence of flowers is also taken as a sign that the seedling has not yet passed its juvenile phase. However, the attainment of the flowering stage and the disappearance of juvenile symptoms does not necessarily occur simultaneously. This appeared clearly from observations on some 400 seedlings, nine to thirteen year old, 92 % of which had flowered at that age, although as much as 78% still showed to a various degree visible signs of juvenility.
In the spring of 1964 these seedlings, which belonged to 71 small progenies originating from crosses made between 1950 and 1954, were visually rated into 5 classes as to their "degree of juvenility" depending on the quantity of thorns present and further on their general appearance of "wildness". This allowed the calculation of the correlation between the degree of juvenility and the length of the juvenile period of each seedling and which appeared to be highly significant as it amounted to +0.52 for 382 seedlings.
TABLE 1. DISTRIBUTION OF APPLE SEEDLINGS IN THEIR 10TH TO 14TH GROWING
IN VARIOUS CLASSES OF JUVENILITY WITH RESPECT TO THE LENGTH OF THEIR JUVENILE PERIOD
|Degree of juvenility||No. of seedlings||% seedlings with a juvenile period (in years) of:|
|1 = no symptoms||84||7||19||28||30||6||6||4|
|2 = low||100||2||11||19||34||24||7||3|
|3 = medium-low||101||0||5||12||31||25||17||10|
|4 = medium-high||73||2||5||3||14||26||30||20|
|5 = high||24||0||0||4||16||21||13||46|
This relation is also illustrated by Table I which presents the distribution of the seedlings. It can be seen that the juvenile period appeared to have been longer when the symptoms of juvenility were more marked at the time of assessment. This means that the seedlings which attain the flowering stage sooner also show a faster rate of modification of juvenile characteristics towards "adult". For example, of seedlings showing no symptoms of juvenility in their 10th to 14th growing year more than half had flowered within 6 years after seed germination, whereas of seedlings which still showed a high to medium-high degree of juvenility only 4-10% had flowered within this period.
The extent to which both parameters are inherent to the progeny to which the seedlings belong can be measured by the correlation between the mean values of each of the 71 progenies for juvenile period and degree of juvenility respectively and which was found to be -0.78 (n = 71). This correlation is highly significant too; moreover, it is significantly larger than the coefficient of +0.52 for all seedlings.
Relation between the average degree of juvenility and the mean length of the juvenile period of 71 progenies of apple seedlings in their 10th to 14th growing year.
The existing relationship is shown by Fig. I. which presents the mean progeny values for the juvenile period as a function of the mean progeny values for the degree of juvenility. It shows that the average degree of juvenility constitutes a fairly close estimate of the mean length of the juvenile period of the progenies.
3.2. Juvenile period and season of fruit picking
SCHMIDT (1947) arranged the seedlings of each of five large progenies (Tables 30-34 in his paper) according to the length of their juvenile period into various classes with respect to the month during which the stored fruits of the seedlings became ripe (edible). He stated that there is no relation between juvenile period and season of fruit ripening. However, this appears not to be quite true for the seedlings as a group, as can be seen from Table 2. This Table shows the distribution of these seedlings and of 340 of our seedlings rated into summer, autumn and winter apples depending on their season of fruit ripening or fruit picking respectively.
TABLE 2. DISTRIBUTION
OF APPLE SEEDLINGS ACCORDING TO THE RELATIVE LENGTH
OF THEIR JUVENILE PERIOD INTO SUMMER, AUTUMN AND WINTER APPLES
|Rel. length of
|No. of seedlings||% of seedlings classified as:|
|Summer apples||Autumn apples||Winter apples|
S data derived from SCHMIDT (1947)
N.B. The correlations
between juvenile period and season of fruit picking or fruit ripening for our
seedlings and those of SCHMIDT were + 0.31 (n = 370) and + 0.30 (n = 1553) respectively.
It is worthy of note that both the correlations and the percentages given in Table 2 are of the same order for the two groups of seedlings. Both sets of data indicate a significant, though weak, relation between the two factors involved. That is to say, a much greater proportion of summer apples is to be found among seedlings with a relatively short juvenile period than among seedlings with a relatively long one, (28-34% versus 0-8%) and vice versa with regard to winter apples (14-26% versus 45-46%); autumn apples are present in about equal proportions (varying between 46 and 54%), irrespective of the length of the juvenile period.
This does not elucidate whether and to what extent the relationship shown also results from inherent differences between progenies originating from different parents.
TABLE 3. THE AVERAGE PERCENTAGE OF APPLE SEEDLINGS FLOWERING WITHIN
6 YEARS IN PROGENIES WHICH HAVE THE SAME PARENT IN COMMON
|Common parent||No. of seedlings1||% flow.2||Common parent||No. of seedlings1||% flow.2|
|Yellow Transparent||124( 9)||63 ± 9.5||Cox's Orange Pippin||77( 8)||22 ±9.8|
|James Grieve||86(10)||62 ± 8.6||Lobo||203( 7)||21 ± 7.0|
|Early Red Bird||42( 5)||57 ± 9.3||Golden Delicious||265(13)||20 ± 7.0|
|Stark Earliest||115(10)||53 ± 9.3||Taunton Cross||343( 6)||15 ± 6.8|
|Jonathan||75( 9)||51 ± 7.1||Ingrid Marie||210( 2)||10 ± 3.0|
1 no. of
progenies between brackets
The correlations derived from our data and those of WELLINGTON (1924) amounted to -0.55 (n = 80) and -0.50 (n = 42) respectively. These significant correlations infer that the relation between picking (ripening) season and juvenile period of the seedlings (see Tables 2 and 3) arises at least partly from inherent differences between progenies.
Table 4, summarizing our data and those of WELLINGTON (1924), shows that the two sets of data are markedly similar. In both cases progenies originating from very early to mid-early parent combinations appear to produce in all instances a significantly higher proportion of seedlings flowering within 6 years than progenies derived from mid-late to very late varieties. The relation between the two factors is apparently not quite linear, which would partly account for the significant, but rather low correlations. The relatively low values are also due to the considerable variation (as indicated by the standard errors 4), caused by "exceptions to the rule", such as e.g. the progenies which had Jonathan as one of the parents (see Table 3).
TABLE 4. THE
PERCENTAGE OF APPLE SEEDLINGS FLOWERING WITHIN 6 YEARS IN PROGENIES ORIGINATING
FROM CROSSES WITH RATINGS VARYING BETWEEN A VERY EARLY AND VERY LATE FRUIT PICKING (RIPENING) SEASON
|Mid-parent rating||No. of seedlings1||% with juvenile period ≤ 6 years2|
66.0 ± 7.79
51.2 ± 10.87
|Early||109(15)||679( 2)||54.1 ± 8.61||43.5 ± 8.49|
|Mid-early||174(13)||363( 8)||42.5 ± 8.06||58.0 ± 8.35|
|Mid-late||191( 9)||359(14)||20.0 ± 5.86||20.5 + 3.78|
|Late||523(23)||418(11)||23.9 ± 4.65||26.8 ± 5.58|
|Very late||279(12)||41( 1)||16.3 ± 6.42||5.0|
|W derived from WELLINGTON (1924)|
|1number of progenies within brackets|
|2percentages with their standard errors|
3.3. Juvenile period and fruit growth period
The existence of a relation between the picking season of the parent fruits and the juvenile period of the progenies is in itself not so easy to understand, nor is the occurrence of a similar relation (r = -0.49 for n = 80) for the mid-parent values for time of flowering and the progeny values for the juvenile period (expressed as a percentage). However, the time of flowering and time of fruit picking are so to speak the functions of the growth period of the fruits of which they constitute the beginning and the end. The strength of this interrelation appears from the correlations, based on the data of the 35 parents varieties used in our crosses, between the fruit growth period of the varieties on the one hand and the time of flowering and of fruit picking respectively on the other and these correlations amounted to +0.76 and + 0.94.
In order to find out to what extent the juvenile period of the progenies also depended on this parameter, the fruit growth period of the varieties was rated into 7 classes at 10-day intervals: 1 = growth period ≤ 95 days, 2 = 96-105 days, .... 7 = ≥ 146 days. This was also done for the parent varieties used by WELLINGTON (1924) on the basis of TUKEY'S (1947) observations at the same Experimental Station on the length of the fruit growth period of a large number of varieties.
The correlations between the mid-parent values, subsequently calculated for the fruit-growth period, and the percentage seedlings flowering within 6 years of the progenies amounted to -0.52 (n = 80) and -0.53 (n = 42) for our data and those derived from WELLINGTON respectively. The correlation, in which the actual mean juvenile period for the progenies was used as a parameter, instead of the juvenile period expressed as a percentage, also amounted to (+)0.53 in the case of WELLINGTON'S data. These correlations are just as significant as those found with the parent characters of season of flowering or fruit picking (ripening) as parameters. They infer that on an average varieties with fruits developing in a relatively short period produce seedlings flowering in a relatively short period and vice versa for varieties the fruits of which need a longer development period.
3.4. Juvenile period and vegetative period
The relatively low values of the correlations with respect to the inheritance of the juvenile period suggest that the parents must possess a property determining this period more specifically than the parameters used so far. Which property may be involved can be guessed when it is remembered that "adult" varieties also have, to use a term from practice, an "unproductive period" and vary as to the age at which they come into bearing. Thus it seems logical to assume that the unproductive period of the parents — defined as the vegetative period — is the more specific factor determining the unproductive period of the progeny — defined as the juvenile period. This could not be confirmed by our own data, as our parent varieties were worked on a precocious stock which greatly reduces varietal differences. However, use could be made again of WELLINGTON'S (1924) data, as his parent varieties were worked on a vigorous seedling stock which causes a much greater variation as to the length of the vegetative period (varying between 4 and 10 years). The length of this period is mentioned by WELLINGTON in the text of his paper, so that the mid-parent values could be calculated and subsequently correlated with the mean juvenile period of the progenies (derived from Table 2 in his paper). The correlation amounted to + 0.77 (n = 42), which is much higher than the correlation of + 0.53 found between the mid-parent values for fruit growth period and mean juvenile period for the same 42 progenies (see p. 130).
This relation also explains the so-called exceptional performance of the "late" variety Jonathan producing early flowering progenies (see Table 3 and p. 129), since this variety is known to come into bearing very soon.
Fig. 2 which presents the mean length of the juvenile period of the progenies as a function of the mean length of the vegetative period of the parent varieties shows that the latter property fairly closely determines the former. This relationship is further illustrated by Table 5 which presents the distribution of the seedlings.
Relation between the mean length of the vegetative period of the parents and the mean length of the juvenile period of 42 progenies of apple seedlings (calculated from data given by WELLINGTON, 1924).
TABLE 5. LENGTH OF THE JUVENILE PERIOD (IN YEARS) OF APPLE SEEDLINGS AS
RELATED TO THE MEAN
LENGTH OF THE VEGETATIVE PERIOD (IN YEARS) OF THE PARENTS (DERIVED FROM WELLINGTON, 1924)
|Mid-parent value for vegetative period||No. of
|% with juvenile a period (in years) of|
It can be seen from Table 5 that e.g. parent combinations which on an average took less than 5 years to come into bearing produced seedlings of which 77% flowered within 6 years, while those originating from parents which came into bearing after 8 or more years, only 5-8% flowered. On the whole Fig. 2 and Table 5 show that varieties which are early reproductive also produce seedlings a high proportion of which are early reproductive, the reverse is true for varieties which come late into production.
4. DISCUSSION AND CONCLUSIONS
From the highly significant correlation between the degree of juvenility and the length of the juvenile period for either individual seedlings or for progenies as groups, it can be concluded that these parameters are genetically related.
Further, significant correlations were established between the juvenile period of progenies and the flowering and fruit picking (ripening) season of the parents. An equally significant correlation existed with the length of the growth period of the parent fruits. This period is in fact a measure of the growth rate of the fruits. Also in view of the interrelation between fruit growth period and time of flowering or fruit picking it may be assumed that the juvenile period of progenies depends on these parent characters only as far as they are indicative of differences in (fruit) growth rate. This assumption is in accordance with earlier observations (VISSER, 1964). These showed the existence of a significant, though rather weak, negative correlation between the juvenile period of seedlings and their trunk-diameter which likewise points to a partial dependence of the juvenile period on the rate of (vegetative) growth.
It is evident, however, from the relatively low values of the correlations that the growth rate is only one of the complex of factors which govern the attainment of the flowering stage. This is also substantiated by the existence of a much higher correlation (0.78 versus 0.53) between the juvenile period of the progenies and the vegetative period of the parents which character apparently comprises more of the factors at stake than the parameters previously mentioned.
With regard to breeding and selection the following tentative conclusions may be drawn.
a. In view of the highly significant correlation between the unproductive period of the parent and that of the progenies, crosses between late-bearing varieties should be avoided. This would give progenies of which many seedlings are likely to come late into bearing with respect to their juvenile as well as their vegetative period and which would retard the breeding program and introduce a characteristic undesirable for cultivation. The crossing of early-bearing varieties has obviously a twofold advantage. The important question whether the property early or late bearing is also genetically linked, with a high or low productivity cannot be answered, but is under investigation.
b. Although the highly significant relation between degree of juvenility and juvenile period was established for older seedlings, there seems to be no reason why this would not also apply to seedlings of a much younger age. If so, an early elimination could be undertaken of those seedlings of a progeny which show a comparatively high degree of juvenile symptoms. Thus one would probably remove a majority of seedlings with the undesired property of "late-bearing" in either the juvenile or the adult phase or in both respects.
c. Since the season of fruit picking of the parents determines the season of fruit picking of the progeny much more significantly than its juvenile period (corr. 0.94 versus 0.55), pre-selection on the basis of juvenile symptoms (length of juvenile period) must be done within the progeny. Pre-selection among seedlings irrespective of their origin would bias the selected group e.g. towards potentially "early" and the eliminated group towards potentially "late" with regard to the fruit picking season of the seedlings.
With regard to the physiological aspects of the observations, there is indirect evidence for presuming that the unproductive phase of (juvenile) seedlings and of (adult) varieties are similar physiological phenomena in which the attainment of the flowering stage is governed by the same or similar factors. This presumption is supported by the following observations.
a. The length of the juvenile period of a progeny is quantitatively determined by the length of the vegetative period of the parents.
b. Measures which reduce or promote growth prolong or shorten the unproductive period of both seedlings and varieties.
c. The interaction between stock and scion is similar for seedlings and varieties, in both cases the scion bears sooner or later depending on which rootstock is used.
d. Certain morphological characteristics shown by e.g. the leaves of seedlings in their juvenile phase can also be observed on leaves of vigorously growing vegetative shoots of adult varieties (MURAWSKI, 1957; SCHWANITZ, 1953; SAX, 1962).
Summarizing our observations, some of which are speculative, it may be concluded that the plant breeder as well as the fruit grower may profit from studies of the genetical and physiological aspects of the juvenile phase; also as such studies may provide a better insight into the factors which determine the length of the vegetative period in the adult phase.
My sincere thanks are due to MR. A. A. SCHAAP and MR. J. D. DAUBANTON for their assistance.