The American Naturalist 56: 66-70 (1922)
The Nature of Bud Variations as Indicated by Their Mode of Inheritance (excerpt)
Professor R. A. Emerson

Cornell University


Several cases of vegetative variation in plants have been studied with sufficient thoroughness to leave little doubt that they are mutations in the strict sense, involving the modification of particular genes. Most of them are concerned with variegated color patterns of flowers, leaves, or fruits, and they are more or less regularly recurrent, a fact that makes them especially well suited to quantitative studies, for it is obvious that a quantitative study can be made only of variations that occur with considerable frequency. For the most part also these somatic mutations are dominant to the type from which they spring, appearing frequently in material homozygous for their recessive allelomorphs, facts that exclude the possibility of their being due to any sort of somatic segregation of unlike genes. Blakeslee's (1920) case of a somatic variation in Portulaca is one of the few examples not involving variegation. Other cases have been reported by Baur (1918).

One of the earliest cases of somatic mutation was reported by deVries in variegated flowers of Antirrhinum. Though the work was done prior to the rediscovery of Mendelism and not discussed from the standpoint of recent genetic interpretation, there is little doubt, as I have noted elsewhere (Emerson, 1913), that the results can best be interpreted as due to a somatic gene mutation.

Correns's (1910) results with respect to the occurrence and behavior in inheritance of green-leaved variations on variegated-leaved Mirabilis and of self-colored flowers on variegated flowered strains of the same species were among the first to be subjected to critical genetic analysis. The behavior in inheritance of green branches of variegated Mirabilis shows this vegetative variation to be a simple dominant mutation affecting ordinarily only one of the duplex recessive allelomorphs. A mutated branch is, therefore, as truly a heterozygote as if it had arisen through hybridization of green and variegated strains.

Self-colored branches on variegated-flowered plants of Mirabilis usually do not transmit the self-color character to their seed progenies in greater percentages than do variegated-flowered branches of the same plants. They are thought by Correns to be fundamentally of the same nature as the green branches of variegated-leaved plants, their failure to transmit the self-color character being due presumably to the accident that the mutation occurs in epidermal cells from which no gametes arise. The frequent occurrence of self-colored plants in seed progenies both of self-colored and of variegated flowers is considered evidence of their origin as vegetative rather than as gametic mutations, their failure of expression in the soma being thought due to their origin in sub-epidermal cells in which these flower colors do not develop.

2 Unpublished data by W. H. Eyster and E. G. Anderson, and by E. G. Anderson and M. Demerec.

Studies of variations in variegated pericarp of maize by myself (Emerson, 1914, 1917) and by Anderson, Eyster, and Demerec,2 involve practically the same results as those so far reported in investigations of other species and afford in addition quantitative data on certain aspects of the somatic-mutation problem not included in other investigations. The genes for variegated pericarp have been shown to belong to a comparatively large series of multiple allelomorphs including those for colorlessness (white seeds), self color of different intensities, and certain definite color patterns of both the pericarp of the seeds and the glumes and paleƦ of the cobs. Variegation is known to be a simple recessive to self color and a dominant to white.

Self-colored seeds whether occurring singly or in groups in variegated ears produce progenies consisting of approximately 50 per cent. self-colored ears, the other 50 per cent. being either all variegated or all white depending on whether the parent was homozygous variegated, V V, or heterozygous variegated, V W, from a previous cross with white. Seeds that are less than wholly self colored throw a correspondingly smaller per cent. of self-colored ears. Self-colored seeds thus produced have, so far as tested, proved to be heterozygous for self color, behaving in later generations exactly as if produced by crosses of self-colored with variegated or with white races.

Certain cultures of self-colored maize produce a few variegated seeds. Such seeds have been observed only on ears that are heterozygous from previous crosses with variegated strains, S V, or with white strains, S W, never from ears that are homozygous for self color, S S. From such variegated seeds, new variegated races have been produced.

These facts are regarded as indicating (1) that the occurrence of self-colored or partly self-colored seeds on variegated ears is due to somatic mutations of the recessive variegation gene to the dominant self-color allelomorph; (2) that only one of the two variegation genes of homozygous variegated maize mutates at a given time; (3) that it is always the variegation gene, never the white one, of heterozygous material that mutates; (4) that the occurrence of variegated seeds on otherwise self-colored ears is due to reverse mutations from the dominant selfcolor gene to the recessive variegation allelomorph; and (5) that only one of the duplex genes of self-color strains so mutates at any one time, for otherwise there would remain no dominant self-color gene to prevent the expression of the mutation as variegated seeds in homozygous self-colored material.

Another type of somatic variation, quite distinct from the self-color mutations discussed above and often termed dark-crown variation, also occurs frequently in variegated maize pericarp (Emerson, 1917). It is quite as striking in appearance as the self-color mutation, but is not inherited, the progenies of the aberrant seeds being in no way different from those of the normal seeds of the same ears. Microscopic examination of dark-crown and of self-color seeds indicates that in the former the epidermis alone is colored while in the latter the epidermis alone remains colorless. The conclusion seems warranted, therefore, that the two types of variation are fundamentally the same, both being true gene mutations, and that the non-inheritance of the dark-crown type is due to the accident that it occurs in epidermal tissue outside the germ tract.

Recent investigations of variegated maize by Eyster and Anderson have established the fact that somatic mutations affecting small areas occur much more frequently than those affecting large areas. Since a mutation arising in a single cell late in development obviously could not affect so large an area as one originating earlier, it follows that mutations in variegated maize occur with increasing frequency in the later stages of ontogeny. It is true, as pointed out by Muller (1920), that given a constant rate of mutation throughout all stages of ontogeny and granting that one cell is as likely as another to mutate, mutations should appear more frequently in the later stages of development because of the fact that there are then many more cells in which mutations may arise. But Eyster and Anderson have found that the increase in the frequency of occurrence of mutations during the progress of development is accelerated far beyond expectation based on the increase in number of cells

This behavior is strongly suggestive of a progressive acceleration in the mutability of the variegation gene as development proceeds. It is much too early to say whether this progressive change, if such it be, is inherent in the organization of the gene itself, as suggested by Anderson and Demerec, or whether it is a response to progressive changes in physiological and environmental relations. Perhaps the assumption of an equal chance of mutation as between any two cells is without sufficient warrant. Possibly there is a time element to be taken into account, as noted by Muller (1920). As cell division becomes progressively retarded in the late growth stages, may not each cell be exposed for an increasingly longer period of time to the chance of mutation? Perhaps it may be possible to test this assumption in favorable material by a comparison of the frequency of mutation in the very early slow-growth, the later rapid-growth, and the final slow-growth periods of the life cycle; but the relatively few cells present in the very early growth period seems likely to place serious limitations on the practicability of such a test. An observation of possible importance in connection with the question of a time element in mutation and with the problem of environmental and physiological influences is that made by Eyster and Anderson concerning the greater frequency of the nonheritable (epidermal) mutations than of the heritable (sub-epidermal) ones in variegated pericarp of maize.

I have recently obtained results bearing on another phase of the somatic-mutation problem as related to variegated maize pericarp, namely, the relative frequency of mutation of homozygous, VV, and of heterozygous, VW, material. It has been shown above that the W gene for colorless (white) pericarp does not mutate, so far as known, when paired either with itself, WW, with the variegation gene, VW, or with the self-color gene, SW. It will be recalled further that only one of the two homologous genes in homozygous variegated, VV, material mutates at any one time. If it could be assumed that the mutability of either allelomorph is uninfluenced by the presence of the other, it should follow that somatic mutations will occur with approximately twice the frequency in homozygous, VV, as in heterozygous, VW, material. But this expectation has not been realized. On the contrary, both heritable (self-color) and non-heritable (dark-crown) mutations have appeared throughout all my cultures with somewhat greater frequency in heterozygous than in homozygous variegated ears. The difference has been especially pronounced in very light variegated strains, where mutations have appeared about two and one half times as often in heterozygous as in homozygous material. Even if mutations appeared with equal frequency in heterozygous and in homozygous ears, the simplex gene of the former must have a mutability of about twice that of either of the duplex genes of the latter. In the very light variegated strains, therefore, a simplex gene must have a mutability of about five times that of a duplex gene.

What appears to be a similar result in Mirabilis has been reported by Correns (1903, 1904). Crosses of a supposedly pure white race with several self-colored pink, yellow, and pale yellow races resulted in every case in plants with strongly red-striped flowers and with numerous self-red flowers or even whole branches of such flowers. Intercrosses of the pink and yellow races gave only self-colored progeny, from which fact it was concluded that the white-flowered race carried a latent factor for striping. It was later discovered that about three per cent. of the flowers of the white race showed minute flecks of red. It was evidently an extremely light, variegated race, rarely if ever throwing somatic self-color mutations when the variegation gene was duplex (homozygous material) but producing such mutations with considerable frequency when that gene was simplex (heterozygous material). Correns concluded that red variegation of Mirabilis flowers is a character that, with self-fertilization or inbreeding, remains almost completely latent, but which, through the entrance of foreign germ plasms, is brought to full expression.

If the mutability of a gene can be increased through the influence of some modifying factor or factors brought into combination with it by crossing, as suggested by Correns, it should be possible to discover crosses that would not produce the effects so far observed in Zea and Mirabilis. While the problem deserves much more study from this viewpoint, it seems unlikely that results with maize can be explained on any such basis, unless the postulated modifying factor is the allelomorph of the variegation gene or some factor very closely linked with it. It must be noted in this connection that the comparison in maize was made between homozygous and heterozygous variegated ears of the same F2 progenies grown from self-pollinated F1 heterozygotes—a circumstance that would afford abundant opportunity for recombinations of independently inherited modifying factors. That the differences in mutability noted in maize may be due to differences in the interaction of like as contrasted with that of unlike allelomorphs, as suggested by Anderson and Demerec, is a somewhat novel conception worth careful consideration if means can be devised for subjecting it to a crucial test.

Before the topic of somatic mutation is dismissed, it should be noted that the phenomenon is not limited to plants. Among animals, Drosophila (Morgan and Bridges, 1919) has furnished several examples of undoubted somatic mutation resulting in mosaic individuals other than gynandromorphs.

CybeRose note: It is interesting to see, so many years after this paper was written, how experts of the time made unnecessary assumptions about the existence of "modifiers" to explain every deviation from the Mendelianist dogma. Why should all the yellow, pink and pale yellow Mirabilis strains carry specialized modifiers that apparently had nothing to do but interfere with the expression of whiteness in a separate strain? And if the occasional self-colored flowers produced on variegated-flowered plants did not produce self-colored offspring, why should we regard the change as a gene mutation? Correns thought (as Emerson noted earlier in this paper) that "their failure to transmit the self-color character being due presumably to the accident that the mutation occurs in epidermal cells from which no gametes arise." Of course, this does not explain why such mutations occur only in epidermal cells.

A more plausible explanation, in modern terms, is that the suppression of red pigment in the white-flowered Mirabilis involves gene silencing involving a transposon. The "genomic shock" that results from crossing with a different strain releases (or partially releases) the suppression, allowing red pigment to be expressed in some cell-lines. Something similar occurs when the Black Mexican sweet corn is crossed with other varieties. Ordinarily the silks, glumes and anthers of Black Mexican are white or pale green; the seeds become fully pigmented only when mature. Cross-bred progeny of Black Mexican express the red pigment in all or most of the silks, glumes and anthers, but not in the seeds — except for occasional black or purple spots.

J Plant Physiol. 2014 Nov 1;171(17):1586-90. Epub 2014 Jul 25.
Transposon-mediated mutation of CYP76AD3 affects betalain synthesis and produces variegated flowers in four o'clock (Mirabilis jalapa).
M. Suzuki, T. Miyahara, H. Tokumoto, T. Hakamatsuka, Y. Goda, Y. Ozeki, N. Sasaki

Abstract The variegated flower colors of many plant species have been shown to result from the insertion or excision of transposable elements into genes that encode enzymes involved in anthocyanin synthesis. To date, however, it has not been established whether this phenomenon is responsible for the variegation produced by other pigments such as betalains. During betalain synthesis in red beet, the enzyme CYP76AD1 catalyzes the conversion of L-dihydroxyphenylalanine (DOPA) to cyclo-DOPA. RNA sequencing (RNA-seq) analysis indicated that the homologous gene in four o'clock (Mirabilis jalapa) is CYP76AD3. Here, we show that in four o'clock with red perianths, the CYP76AD3 gene consists of one intron and two exons; however, in a mutant with a perianth showing red variegation on a yellow background, a transposable element, dTmj1, had been excised from the intron. This is the first report that a transposition event affecting a gene encoding an enzyme for betalain synthesis can result in a variegated flower phenotype.

Euphytica 24(2):323-332 (Jan 1975)
Investigations of the inheritance of flower variegation in Mirabilis jalapa L. 6. Genetic system of flower variegation and speculation about its existence.
J.M.M. Engels, W.N.M. Van Kester, C.J.T. Spitters, et al.

A genetic model for flower variegation in Mirabilis jalapa is given. Two loci effecting pigment production are assumed. The dominant alleles of each of these two loci may be repressed and thus they do not express themselves. In the presence of a dominant variegation gene a repressed allele can become active at some phase of the ontogeny of the plant. Repression and later release of repression results in a pattern of variegation of a dominant colour phenotype on the background of a recessive colour phenotype. Some parallels are drawn between the gene controlling system in M. jalapa and that in maize. In conclusion a practical application for plant breeding is given.

Bazavluk found some odd results when pollinating white Mirabilis jalapa with pollen mixtures that suggest a cross influence between neighboring embryos, or between pollen-tubes in the same style.

Mirabilis bibliography