Nature 181: 928-929 (29 Mar 1958)
Environmental Conditioning of Flax
Department of Agricultural Botany, University College of Wales, Aberystwyth.

EXPERIMENTS carried out over a number of years have shown that remarkably large differences can be produced in the weight of flax plants as a result of the effect of the environment on previous generations of plants. In one experiment, all eight combinations of nitrogen, phosphorus and potassium fertilizer treatments were applied to forty plants of an inbred, self-fertilizing variety in the damp, dull season of 1954. The progeny, which were grown under a uniform set of fertilizer treatments, were cut at ground-level at maturity and weighed. The differences in the weights of the progeny (C1 1955) due to the parental treatments are shown in Table 1. Some types are as much as two and three times the weights of others and, with the exception of the nitrogen plot, they are closely correlated with the weights produced by applying the fertilizers directly to the plants (Table 1, C0 1955).

The differences were undiminished in the second generation grown in 1956 (C2 1956), although the seed obtained from the first generation was of the highest quality in weight, appearance and germination, and the C1/C2 correlation was virtually complete (r = 0.97). In another test on the second generation grown in 1956, 960 Plants descended from plants receiving nitrogen and potassium two generations earlier weighed 0.85 cwt., and an equal number descended from plants receiving phosphorus and potassium weighed 2.63 cwt.—three times as much. The difference of 1.78 cwt. had a standard error of 4.1 lb. Again there was no difference in seed weight, germination capacity or energy, and the plants themselves within each type were highly uniform. Large differences have also been observed in the third generation and there is evidence from young plants that they occur in the fourth generation.

The experiment was repeated by applying the same set of fertilizers in the warm, sunny season of 1955, but this time the effect on the progeny grown in 1956 was much less (Table 1, C1 1956), although the differences wore still significant and, apart from the nitrogen plot which was exceptional before, substantially the same. Evidently seasonal factors are as important as nutrition. This was also demonstrated by another experiment in which plants from seed collected in 1955 were, for comparable fertilizer treatments, twice the weight of plants from seed collected in 1956, when the two sets of plants were grown together in 1957.

    NPK NP NK N PK P K Nil S.D. x t
C0 1955 11.4 11.8 4.4   6.1   9.6 10.4   8.9 7.3 3.3
C1 1955 11.l   9.5 3.7 12.l 11.3   8.4   7.8 5.9 1.2
C2 1956 17.5 15.9 6.5 18.7 15.5 14.2 12.4 8.1 3.3
C1 1956 11.6   9.2 8.2   7.8 10.9   9.3   8.2 8.2 2.2

The inheritance of such large differences to at least the fourth generation is likely to be due to cytoplasmic change rather than to maternal effects, and this is supported by other experiments. (i) Plants were grown from seed from capsules collected at varying stages of ripeness. Plant weight increased logarithmically with decrease in seed weight to the limit where the seed was so small that no germination occurred. (ii) Forty plants of two conditioned types which were reciprocally grafted retained their identity in both stock and scion. (iii) Reciprocal crosses between two conditioned types resembled the female parents more than the male, but there was also clear evidence of transference of effect through the pollen in both directions. (iv) The conditioned types do not produce the same relative dry weights when grown in the field in the summer as in a warm greenhouse under the lower light intensity and shorter day of winter. Presumably the types are adapted to different environments.

One of several reasonable hypotheses which can be put forward at this stage is that, with relatively high temperature and low light intensity, cell division can proceed rapidly; but the number of cytoplasmic self-duplicating particles falls, due to a shortage of photosynthetic products, the utilization of these products being also influenced by mineral supply. The altered cytoplasm stimulates the nucleus to synthesize different substances, or different amounts of the same substances, to establish a new equilibrium between nucleus and cytoplasm. The new equilibrium could be at least as stable as the old, and the new plant type to which it gives rise would have the appearance and constancy of a distinct genotype. Such a cytoplasmic-nuclear interaction may further simulate genetic change by the nuclei themselves having an effect on the difference between reciprocal crosses of environmentally conditioned types, the pollen nucleus complementing any small effect of the pollen cytoplasm. In short, plants may remain differentiated as a whole over several generations in addition to the normal differentiation of plants  within a generation. Temperature/light relations will probably play an important part in further investigations.

A detailed account of these studies on flax, and on other organisms, will appear in due course. This work was aided by a grant from the Agricultural Research Council.

Fourth generation plants of two extreme types of flax induced by fertiliser treatments. Left, npk; right, nk.

Illustration from Durrant, A. (1962) The environmental induction of heritable change in Linum. Heredity, 17: 27-61.