Journ. of Genetics, 1: 47-56 (1910)
THE MODE OF INHERITANCE OF STATURE AND OF TIME OF FLOWERING IN PEAS (PISUM SATIVUM).
BY FREDERICK KEEBLE,
Professor of Botany, University College, Reading;
AND MISS C. PELLEW,
Research Student, Botanical Laboratory, University College, Reading.

THE experiments recorded in the present paper, though incomplete, throw some light on the nature of the Mendelian factors which determine stature in peas (Pisum sativum) and on the mode of inheritance of earliness and lateness of flowering in this species. The experiments were designed originally to investigate the latter problem—left undecided by Mendel's classical experiments on the inheritance of "time of flowering." As our work proceeded, it became evident that this function of the plant is not unconnected with certain, definite, morphological characters. Hence it becomes necessary to follow the course of inheritance of these characters, e.g. length of internode and thickness of stem. In doing this, we have been led to conclusions concerning, not only the relation of these morphological characters with flowering period, but, also, the part which these characters, play in determining the stature of peas. We deal first with the latter point.

Stature. Certain garden races of Pisum sativum grow tall and give rise to tall-growing offspring; other races are dwarf and breed true to this character. Adopting Bateson's classification (1909, A) we call "tall," those varieties which grow 5–6 or more feet high, "dwarf," those which range from 9 inches to 3 feet. Between dwarf and tall are various "half-dwarf" races which reach a height of about 4 feet. The actual height attained by the various races is determined in any given year, partly by gametic constitution and partly by the external conditions to which the plants are subjected during their growing period. Thus the two half-dwarf varieties Autocrat and Bountiful, used in our experiments, are so constant with respect to stature as to be described by Messrs Sutton and Sons, to whom we are indebted for seeds, as being, the former variety 3–4 feet, the latter 3 1/2–4 feet in height. Nevertheless, during the constantly wet summer of 1909 both Autocrat and Bountiful reached in the College Gardens at Reading an average height of 5–6 feet. We refer to these well-known seasonal fluctuations in height in order to point out that particular care is required in the interpretation of the results obtained in any one year and in the comparison of the statures of plants grown during different years.

The cross Autocrat and Bountiful and its reciprocal. This cross, made in 1907, and repeated in 1908, yielded an F1 generation, the plants comprising which were considerably taller than either parent grown under like conditions. The average height of F1 plants was 7–8 feet, that of the parent plants 5–6 feet.

F1 selfed, yielded offspring which ranged in height from 8 feet down to 1 1/2 feet. In all, 192 F2 plants were recorded. Of this number, 61 plants were the progeny of a single F1 plant of Autocrat x Bountiful grown in 1908. The remaining 131 plants of the F2 generation were descended from four F1 plants of the cross Bountiful x Autocrat The seeds from these four plants were, owing to a mistake, harvested together. There is, however, no recognisable difference between the descendants of the single family from Autocrat x Bountiful and those derived from the four F1 plants of Bountiful x Autocrat. We will therefore consider the 192 F2 plants as a whole.

The F2 plants, showing such marked differences among themselves with respect to height, fall into four groups which, for the moment, may be defined as follows:—F1 type, Autocrat type, Bountiful type, and Dwarf type. Moreover, when classified in this way, the numbers of plants in the four groups show a close approximation to those expected in the F2 generation derived from a dihybrid cross; that is one in which two pairs of characters are involved.

Thus; F2 =              
  F1 type   Autocrat   Bountiful   Dwarf
Observed 114   33   32   13
Calculated 108   36   36   12
  9 : 3 : 3 : 1

Inspection of the parent plants, Autocrat and Bountiful, reveals the fact that, besides other, apparently minor, differentiating characters, these two half-dwarf varieties, are distinguished from one another by two well-marked characters, namely, length of internode and thickness of stem. Thus Autocrat, whose normal height is 3–4 feet, has thick stems (with large fleshy foliage of a bluish green colour) and short internodes of about 3 inches in length. Bountiful, whose normal height is 3 1/2–4 feet, has thin stems (with foliage smaller than that of Autocrat and of a yellowish green colour) and long internodes (5–7 inches). It may be noted incidentally that the rates of growth of these two varieties are very different; the growth in length of the axis of Autocrat being markedly slower than that of Bountiful. For example, when Autocrat and Bountiful are planted at the same time, Autocrat grows one foot whilst Bountiful grows two. The slowness of growth in length is associated with short internodes. The two varieties differ also with respect to mode of branching. Autocrat forms three to five branches at or near the ground-level. These branches develop at the same rate till they and the main axis are about 2 feet in height and then one axis takes the lead. Bountiful shows a less fixed mode of branching. Among the 1909 plants, some branched at the ground-level (2–4 branches), others formed their first branches a foot or so above the ground-level. Generally speaking, thick stem appears to be associated with branching, and thin stem with single stem, at the ground-level. We are engaged in endeavouring to work out the anatomical bases for thick as opposed to thin stem, and for long as opposed to short internodes, and the bearing of these factors on growth.

We will new consider the factors, thickness of stem and length of internode, in relation with stature. That these factors may be taken as valid representatives of those which determine height is evident from the following considerations:—

F1 plants, 7–8 feet high, have all thick stems with long internodes (6–9 inches). If the factor for thick stems is represented by T, and its allelomorph (thin stem) by t, and if the factor for long internodes is represented by L, and its allelomorph (short internode) by l: then the gametic constitution of Autocrat is Tl, that of Bountiful is tL, and hence the gametic constitution of F1 = TtLl. We ascribe the great height of F1, plants to the presence of the factors T and L and to their dominance over t and 1. The suggestion may be hazarded that the greater height and vigour which the F1 generation of hybrids commonly exhibit may be due to the meeting in the zygote of dominant growth-factors of more than one allelomorphic pair, one (or more) provided by the gametes of one parent, the other (or others) by the gametes of the other parents. This provisional interpretation of increased vigour of F1 plants, has at all events the merit of being less obscure than the hypotheses which are current in the literature of plant physiology (Jost, 1907).

We return now to the F1 of the crosses between Autocrat and Bountiful. Since the constitution of F1=TtLl, its gametes have constitutions:— TL:TI:tL:tl, and hence, when F1 plants are self-fertilized, we expect the usual 9:3:3:1 ratio; i.e. in 16 plants, 9 with both dominants (T and L); 3 with one dominant; 3 with the other and 1 with the two recessives (t and l). That the expectation is realised is seen from the following table in which the results already given are recorded in terms of Tt and Ll.

F2=              
  F1 type   Autocrat   Bountiful   Dwarf
  TL   Tl   tL   tl
Observed 114   33   32   13
Calculated 108   36   36   12
  (9 : 3 : 3 : 1)

Of the 13 dwarf (tl) plants, all but one were below 3 feet in height, the three dwarfest being respectively 1 1/2, 1 3/4, and 2 feet. Table II gives the records of height, of thinness or thickness of stem, and of length of internode of the plants which we regard as true dwarfs. The classification is of course open to the objection that thick and thin are but qualitative terms, and that, in difficult cases, the criteria are purely subjective. An answer to this objection is that the records in Table II were made before we were aware that the characters "thin" or "thick" were of any considerable importance. We include in Table II the records of the characters of F2 plants of a stature up to 4 feet. A comparison of the descriptions of the sterns of the shorter plants (above the horizontal line in Table II) with those of the stems of the less short plants (below the line) confirms, as we think, the view which we have expressed above, that the dwarf plants have thin stems and also short internodes. With regard to the range of variation in height, both among the dwarfs, and among the plants of the constitution Tl, it is probable that the character of number of nodes, and also that of the position of the first flowers, are also of importance. It is hoped that further investigation of these characters among the F3 families will determine this point.

We conclude from the above experiments that tallness in peas (P. sativum) depends on the presence of two factors, long internode, and thick stem: that these factors are Mendelian in their inheritance; being dominant respectively to short internode and thin stem factors. Half-dwarf peas are of two kinds. One kind, represented by Autocrat, owes its semi-dwarfness to lack of the long internode factor. In the absence of this factor, the thick-stem factor cannot effect more than a sturdy, medium growth. The other kind of semi-dwarf lacks the thick-stem factor, and, in the absence of this factor, the long internode factor cannot build the stem-segments of a sufficient length to produce tallness in the plant. It may be urged that this, after all, is but a common-sense view of the way in which growth in length is effected: that only plants with long internodes among annuals are likely to be tall; and that only when stems are sturdy may internodes reach their full length. This may well be and it is certainly not a reproach to Mendelism that it may lead to the discovery of the obvious which, without the method, remains obscure.

The conclusions which we have reached as to the gametic constitution of tall, semi-dwarf and dwarf peas may be summarised thus:—

Tall = TL
Semi-dwarf = tL or Tl
Dwarf = tl

In a cross described by Lock (1905) we have what seems to us an interesting confirmation of this view of the chief factors involved in stature of Pisum. Lock's comment on the case is as follows (op. cit. p. 414):—"This cross seems to afford an example of remarkable intensification of both the allelomorphic characters of the same pair, viz. tallness and dwarfness—the former in F1 and both in F2 and later generations." The cross in question was one between Satisfaction—a variety which at Peradeniya grew to an average height of 4.6 feet—described as of robust growth (which we may take to mean thick stem), and with internodes of an average length of 1.74 inches, and a Native Pea of less than 3 feet in height, but varying much in different years, with thin stem, and internodes of an average length of 1 1/2 inches. In the four plants of the F1 generation, the internodes were of an average length of 2.4 inches—longer than in either parent—the height of the F1 plants was about 6 feet, and the number of internodes was the same as in Satisfaction. It would seem that in the increased length of internode of the F1 plants (an average of 2.4 inches as compared with the 1.74 inches of Satisfaction) is seen the influence of thick stem on an internode which, when combined with thin stem, is of an average length of 1 1/2 inches. In F2, the preponderating type resembled the F1 plants, and the appearance of dwarfs, shorter than either parent, with internodes of 1.0–1.2 inches in length (the proportion of long to short being 19:6), confirms our belief that the characters thick and thin stem, long and short internodes were the chief stature-factors involved in this cross. Probably the difference in the number of nodes introduces a complication, but the small numbers grown in F2 and the lack of further records, prevent a full analysis. We should mention that this cross was made primarily by Mr Lock with the object of investigating the characters of the testa of the seeds of Pisum.

In conclusion, with respect to the question of tallness and dwarfness, it is evident that a closer investigation will reveal facts of great importance to an understanding of the physiology of growth.

Time of flowering: earliness and lateness. Certain varieties of peas are well known and prized for their stability with respect to time of flowering, and therefore it is to be supposed that the character is hereditary. Mendel many years ago commenced experiments with a view to determine the mode of inheritance, but few records of these experiments are left to us. In Mendel's memoir on the hybridizing of peas (1909B) we find the following:—"As regards the flowering time of the hybrids the experiments are not yet concluded. It can, however, already be stated that the time stands almost exactly between those of the seed and pollen parents, and that the constitution of the hybrids with respect to this character probably follows the rule ascertained in the case of the other characters."

By the use of the varieties Autocrat and Bountiful for such an experiment, the advantage is gained of a long space of time between the flowering periods of the two varieties: the former variety flowers, in normal seasons, about 30 days after the latter. Thus, in 1909, from sowings made in April, 23 out of 28 plants of Bountiful were in flower on June 2nd, whereas Autocrat, sown at the same time, was only just coming into flower on June 30th (see Table I). In spite, however, of the favourable nature of our material with respect to the character under consideration, we cannot claim to have arrived at a complete understanding of the mode of inheritance of earliness or lateness of flowering. Nevertheless, we publish our records, and our attempts to analyse them in Mendelian terms, since they appear to show definitely not only that the problem is capable of solution, but also the nature of the difficulties which have to be met before the solution is obtained. It will be seen from the records of the time of flowering (Table I) that the F1 generation is intermediate with respect to time of flowering between the parents Autocrat and Bountiful. In 1909, whereas 23 out of 28 plants of Bountiful blossomed by June 2nd, and whereas Autocrat was beginning to flower by June 30th, 10 of the plants of F1 (of a total of 12) were in flower by June 21st; and the remaining plants were in flower by June 30th. The F1 plants of Autocrat crossed Bountiful and those of the reciprocal cross, grown in 1908, confirm this result. From the appearance of such an intermediate form in F1, it may be supposed, either that there is incomplete dominance of lateness over earliness, or that there are two (or more) factors connected with the time of flowering; the meeting of the two, or more, dominant and antagonistic factors, from either parent in the F1 plant, giving an intermediate time of flowering. In the former case, the F2 plants, obtained by selfing F1, may be expected to give the 1:2:1 ratio; but, though segregation of early and late occurs in F2, it is not of this simple type. If we tabulate the observations on time of flowering, not of the F2 generation as a whole, but of the several categories of that generation, viz. thick long (TL), thick short (Tl), thin long (tL), and thin short (tl), we obtain the results shown in the accompanying Table.

TABLE I

The Accelerating Influence of Long Internodes on Time of Flowering of F2 Plants.
(Times of Flowering of Bountiful, Autocrat and F1 are given for purposes of comparison.)

Numbers of Plants in Flower
F2        

Thick
Long
Thick
Short
Thin
Long
Thin
Short
Date of
Flowering
Bountiful Autocrat F1
5 1 24 6 June 2 23
17 1 7 2 June 10 5
48 5 1 3 June 17 8
36 16 1 June 21 2
8 10 June 30 2
1 July 6 (a few
beginning
to flower)

These results show that plants with long internodes, of both thick- and thin-stemmed types, flower, on the whole, earlier than the short internode types. Since long internode is dominant to short internode, F1 plants may be subject to the same accelerating influence with respect to time of flowering as those of the groups, long thick and long thin, We suggest therefore that lateness is dominant to earliness, and that the reason why the plants of F1 flower before those of the late parent Autocrat, is that they possess the factor for long internodes, their gametic constitution being TtLl. The fact that the position of the flowers on the stem, in F1 plants, is about the same as in Autocrat, lends some support to the view that late is dominant to early. There was however a considerable range of variation in this character, both in Autocrat and in the F1 plants. Moreover, owing to the branched habit of Autocrat and of the F1 plants, and to the fact that this character was not considered until rather late in the season, it was impossible in some cases to recognise the main stem, i.e. the stem which flowered first, and this may have spoilt the records to some extent. This character of the position of the first flowers on the stem has been supposed to indicate time of flowering (1905B). Our records show that Autocrat bears its first flowers, on the average, at the thirteenth node, Bountiful at the seventh node, and the F1 plants at the twelfth. Many records of this character were made among the F2 plants. The average result of these records points to the conclusion that low-flowering indicates earliness, high-flowering lateness, but there were many exceptional cases among individuals. Further investigations among F3 families, homozygous in respect of the many other characters involved, should provide a solution to this question.

Proceeding then on the basis that lateness is dominant to earliness, we observe, in the F2 generation, that the flowering period spreads over more than a month, from June 2nd—July 6th, that whereas many (36) plants of F2 flower as early as the early parent, few flower so late as Autocrat (Table I). That time of flowering is influenced by seasonal conditions is undoubted; but the marked differences in flowering-time between the various plants of F2 show that the mode of influence of a given season is determined to a surprising degree by internal factors. A more detailed examination of the distribution of earliness and lateness of flowering among the F2 plants, brings out several facts which lend support to the conclusions that time of flowering, though inherited, is modified in its expression in the zygote by morphological characters such as thickness of stem. As we have shown, the F2 plants group themselves into four classes:—thick long (TL), thick short (Tl), thin long (tL), and thin short (tl). If we chose arbitrarily the date of flowering of Bountiful (June 2) as early and regard for our immediate purpose all plants flowering after this date as late, we find, on scrutinizing the distribution of lateness and earliness among these classes, that most of the thick-stemmed plants with short or long internodes, are late (141 late, 6 early); that, of the thin, short-noded plants, 6 are early and 7 late, and that of the thin, long internoded plants, 24 are early and 8 are late. It is therefore apparent that there is a relation between morphological, vegetative characters and period of flowering. Thick-stemmed plants contain a very high proportion of late plants, thin-stemmed plants contain an almost equally large excess of earlies. As has been shown by Bateson, departures from normal, Mendelian expectation which manifest themselves by discriminate distribution of a character among the members of a generation, may be interpreted by the aid of the hypothesis of gametic coupling. Applying this hypothesis, and assuming that the coupling between thick stem and late factor is of the 7:1:1:7 order (Bateson, 1909, op. cit. p. 159), we arrive at the following results

  TLE TLe TlE Tle tLE tLe tlE tle
Calculated on trihybrid scheme 81 27 27 9 27 9 9 3
Observed 109 5 32 1 8 24 7 6
Calculated on 7: 1 coupling 99.6 8.4 33.2 2.8 9.2 27.6 2.8 8.4
T=thick stem,     L=long internode,     E=late flowering.

Though the numbers are not large enough to demonstrate the existence of 7:1 coupling between thick stem and late flowering factor, yet their general run and fairly close approximation to those expected on the basis of such coupling make it probable, in our opinion, that these two factors are connected with one another in this manner.

The nature of the influence exerted by the long-stem factor in inducing precocity of flowering we are not yet prepared to discuss, nor can we deal with the general physiological problems suggested by these observations; but will content ourselves with pointing out that, before a full analysis of physiological properties such as those of time of flowering can be made, a not inconsiderable amount of breeding work must be done with the preliminary object of obtaining suitable material, i.e. material which consists of groups alike in all respects save in the one which it is proposed to investigate. We learn from the foregoing preliminary experiments that it is not enough to cross any late with any early pea, for, as is indicated by these experiments, lateness and earliness are connected, in a manner not to be suspected on a priori grounds, with definite, morphological, vegetative characters.

The authors have pleasure in acknowledging that in carrying out their experiments they have been aided by a grant from the Royal Society.

TABLE II

Autocrat x Bountiful and Reciprocal Cross.
Description of F2 plants of Heights between 1 1/2 and 4 feet.

Label Date of
Flowering
Height Stem Length of
Internode
  Foliage D=Plants
reckoned
as Dwarf
5x3/5/10 June 2nd 1 1/3 feet Thin 3 inches   Very small D
3x5/2/60 " 9th 1 3/4 " Thin 2 3/4 "   Bountiful type D
3x5/2/43 " 2nd 2 " Thin 3 "     D
5x3/6/7 July 6th 2 1/2 " Thin 1 1/2 "   Very small D
5x3/6/8 June 2nd 2 1/2 " Thin 2 "   Small (=Bount.) D
5x3/4/34 " 2nd 2 1/2 " Thin 2 " ? Intermed. D
5x3/2/4 " 2nd 2 1/2 " Thin 2 "   Bountiful D
5x3/4/19 " 16th 2 1/2 " Thin 3 "   Small D
3x5/5/34 " 30th 2 1/2 " Thick 5 " ? Intermed.  
5x3/6/6 " 10th 2 3/4 " ? Thin 2 " ? " D
3x5/2/20 " 2nd 2 1/2–3 feet Thin 3 "   Bountiful D
5x5/2/34 " 21st 2 1/2–3 " ? Thin 4 "   Autocrat D
5x3/2/14 " 16th 2 1/2–3 " ? ? " ? Bountiful D
5x3/5/12 " 16th 3 " ? Thin 3 "   Intermed. D

5x3/5/41 " 21st 3 " ? Thin 4 "   Diseased  
5x3/1/5 " 21st 3–3 1/2 " ? Thick 3 "   ?  
5x3/3/5 " 30th 3–3 1/2 " ? Thick 3–3 1/2 inches   Small  
5x3/1/10 " 16th 3 1/2 " Thick 3 1/2 "   Small (=Bount.)  
3x5/2/8 " 16th 3 1/2–4 " Thick 3 " ? Autocrat  
3x5/2/52 " 2nd 3 1/2–4 " ? Thick 4 "   Autocrat  
5x5/4/29 " 21st 3 1/2–4 " ? Thick 4 " ? Autocrat  

REFERENCES CITED IN TEXT.