Genetics, Vol. 150, 957-961, November 1998, Copyright © 1998
Marcus Rhoades and Transposition
Nina Fedoroffa
a Pennsylvania State University, University Park, Pennsylvania 16802
Corresponding author:
Nina Fedoroff, Biotechnology Institute, Pennsylvania State University, 519 Wartik Lab., University Park, PA 16802-9807., nvf1{at}psu.edu (E-mail).
Barbara McClintock deservedly received the lion's share of recognition for the discovery of transposition, including the 1983 award of an unshared Nobel Prize in Physiology or Medicine (FEDOROFF 1994 
). But discoveries are punctuation marks in the discourse of science, and many voices impinge on the discoverer's ear. McClintock studied genetics at Cornell. The Cornell genetics group was headed by R. A. Emerson. Marcus Rhoades undertook graduate work at Cornell not long after McClintock's graduation and learned cytogenetics from her (SCHWARTZ 1993 ). But more than that, Rhoades took important steps on the road to the discovery of transposition before, and quite independently of, McClintock's final sprint. And while hindsight has a certain blinding clarity unavailable to the discoverer, there is always an intellectual framework into which a discovery fits. My purpose is to sketch that framework for the discovery of transposition, here emphasizing Rhoades' work on the Dotted (Dt) locus of maize. The year 1998 marks the 60th anniversary of the publication of Rhoades' paper in GENETICS reporting seminal work on the properties of a gene with a transposon insertion, carried out a decade before McClintock's identification of the transposable Dissociation (Ds) locus in maize.
The fact that Rhoades and McClintock were friends and colleagues who corresponded extensively is important to the discovery of transposition. This fertile ground will be tilled in time by historians and, perhaps, biographers. But it is important only because Marcus Rhoades was both an outstanding maize geneticist and because he had himself worked on the genetics of unstable mutations, making observations parallel to those of McClintock. The story doesn't begin with Rhoades either, of course, and a crucial earlier chapter was contributed by Emerson, whose papers were undoubtedly read by both Rhoades and McClintock. Emerson's work, in turn, was rooted in earlier observations on what were initially called "mutable" or "unstable" genes and "ever-sporting" varieties exhibiting variegation for flower and leaf color in plants.
 | Variegation |
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Studying pigment variegation in Antirrhinum, de Vries developed the concept of ever-sporting varieties, concluding that the tendency to variegate was heritable (DE VRIES 1905 ). He noted that the few fully pigmented progeny arising from variegated plants sometimes show heritability of the trait and sometimes give rise instead to progeny that are once again variegated. Correns, working with Mirabilis jalapa, and East and Hays, studying variegation in Zea mays, reported on the other hand that somatic mutations from a variegated to a fully colored phenotype showed Mendelian inheritance (CORRENS 1910 ; EAST and HAYES 1911 ). In any event, the picture was far from clear, and variegation was a phenomenon that was difficult to fit into the newly emerging Mendelian framework. Indeed, EMERSON 1914 opened his first important paper on the genetics of variegation with the striking statement that "Variegation is distinguished from other color patterns by its incorrigible irregularity" (p. 87).
Emerson studied the heritability of pericarp variegation in what was known as "calico" corn (EMERSON 1914 ). Ears produced on plants grown from variegated kernels generally show one of a variety of patterns of striping, but the red area varies considerably, and both colorless and fully pigmented kernels are produced frequently. Emerson took an approach somewhat different from that of de Vries, asking whether there was a relationship between the amount of red-pigmented tissue in a given kernel and the number of red ears produced upon self-pollination in subsequent generations. The clear answer emerged: the more red there was in the kernels planted, the larger the fraction of red ears in the progeny (EMERSON 1914 ). Emerson further found that red kernels produced plants that were commonly heterozygous for the red and variegated traits. He concluded: "The development of red in the pericarp is evidently associated with and perhaps due to a modification of some Mendelian factor for pericarp color in the somatic cells" (p. 102).
In this way, Emerson captured variegation within the Mendelian paradigm, adding the important insight that a somatic change could occur in a Mendelian factor, becoming a heritable change that obeyed simple Mendelian principles. But he readily admitted that it was "utterly impossible at the present time to conceive of the cause or even the nature of this change." Nonetheless, he speculated that the genetic factor for variegation might be "a sort of temporary inhibitor, an inhibitor that sooner or later loses its power to inhibit color development, a power that once lost is ordinarily never regained" (EMERSON 1914 , pp. 112–113). Emerson's idea was that variegation was due to the association of some kind of a genetic factor with a locus and that its loss was what allowed the gene to be reexpressed. Emerson subsequently reported that occasional variegated kernels appeared on otherwise fully pigmented ears. This suggested that at some low frequency, the inhibitory factor might once again become associated with the gene, then called a "unit factor" (EMERSON 1917 ). Emerson viewed variegation as a reversible change in an otherwise conventional gene, distinguishing itself from other kinds of mutations by its high frequency. Thus, Emerson had not only made variegation intelligible in a Mendelian context, but had deduced that it was caused by a modification in the structure of the gene.
Emerson later made some puzzling observations that were to remain unexplained until McClintock's studies decades later (EMERSON 1929 ). First, he made the counterintuitive observation that reversion to wild type was less frequent when the variegating pericarp color gene was homozygous and therefore present in two copies than when it was heterozygous with a stable nonpigmenting allele. Second, he noted that chromosomes carrying a stable, recessive, nonpigmenting allele of the pericarp color locus recovered by segregation from a variegating heterozygote show some ability to suppress variegation when again used to create a variegating heterozygote. As explanations of the latter, he entertained the radical hypothesis that information is transferred between alleles either as "a direct contamination of one allelomorph by another" or by transfer of "distinct gene elements" from one allele to another (EMERSON 1929 , p. 506). But he readily admits that he, the writer, "is wholly unable to devise a consistent working hypothesis to account for his results on any such assumption" and suggested the alternative hypothesis of distinct modifiers of variegation, which had already been reported in Drosophila virilis (DEMEREC 1928A ).
| Mutable genes |
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The view that variegation is attributable to ordinary mutations occurring at a high frequency was challenged over the next decade as mutable genes were studied in both Drosophila and plants (DEMEREC 1928B , DEMEREC 1929 , DEMEREC 1931 , DEMEREC 1935 ; STERN 1935 ; RHOADES 1936 ; PLOUGH and HOLTHAUSEN 1937 ; RHOADES 1938 , RHOADES 1941 ). Goldschmidt proposed that mutations are a consequence of position effects, and both he and Correns believed that mutable genes are sick or diseased genes and that any conclusions derived from their study were not applicable to other types of mutations (GOLDSCHMIDT 1938 ). Rhoades and Demerec, on the other hand, shared Emerson's view that there was no clear-cut difference between stable and unstable genes.
In 1936, Rhoades reported a seminal observation, one that has withstood the test of controversy and time. He identified and isolated a "dotted" allele of the A1 locus of Z. mays from an ear of Black Mexican sweet corn whose original segregation ratio suggested that the variegating dotted character required both the recessive a1 allele and a second locus (RHOADES 1936 , RHOADES 1938 ). He then showed clearly that variegation depends on two different loci, one that he designated the Dt locus and the other that appeared to behave like a standard recessive a1 allele in the absence of the Dt locus (RHOADES 1938 ). Curiously, this apparently new a1 allele proved indistinguishable from the standard stable recessive a1 tester allele originally isolated by Emerson and used for two decades without showing evidence of variegation (EMERSON 1918 ; RHOADES 1938 ). Rhoades showed that the Dt locus was not linked to the A locus and that both the standard and newly isolated a1 alleles exhibited variegation or mutability only in its presence.
Thus, Rhoades had identified a gene that destabilized what appeared to be an ordinary stable mutation. Knowing nothing about the mechanism, he hypothesized that the normally stable a1 allele mutated to A1 in the presence of Dt (RHOADES 1938 ). He suggested that each dot of color represented one mutation and, therefore, that the number of dots reflected the mutation frequency and the sizes of the dots reflected their timing in development. Rhoades predicted that mutations that occur in sporogenous tissue that gives rise to gametes should be genetically transmissible. In a plant that was homozygous for a1 and Dt and had the appropriate genetic constitution at other loci affecting pigmentation, Rhoades observed purple anthers and anther sectors. Using pollen from such anthers, he assessed the frequency of transmission of the putative A1 alleles and observed that half of the fully pigmented anthers he tested were A1/a1 heterozygotes. This observation supported his hypothesis. He also noted that, unlike the unstable a1 allele, the A1 allele derived by mutation from a1 was stable and did not revert to the unstable a1. Rhoades further ascertained that the effect of Dt was quite specific to the a1 allele and had no effect on the mutation frequency of recessive alleles at other loci, including the pericarp color allele Emerson had studied, by then designated Pvv (RHOADES 1941 ).
Rhoades concluded that whether a mutation is stable or unstable can be a function of the genetic background. Having looked for and failed to find chromosomal abnormalities, he dismissed a mechanical explanation, such as chromosome loss or rearrangement, as an explanation for the ability of Dt to destabilize the a1 allele. To explain his observation that the frequency of mutations from a1 to A1 increases linearly with the number of a1 gene copies and exponentially with the number of copies of Dt, he suggested that the Dt gene produced something that accelerated mutation of a1 to A1 (RHOADES 1938 ). Although McClintock's first experience with transposable elements was through the analysis of a chromosome breakage phenomenon rather than an unstable mutation, she knew the behavior of the Dt-a1 system and recognized the similarities early.
| Chromosome breakage |
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McClintock's discovery of transposition had its origins in her studies on the behavior of broken chromosomes. Her objective was to understand the behavior of a chromosome with a broken end during mitotic divisions and she found that chromosomes lacking telomeres do not separate during replication, thus producing dicentric chromosomes. The dicentric chromosomes break, regenerating chromosomes with broken ends and establishing what McClintock referred to as the "breakage-fusion-bridge" cycle (MCCLINTOCK 1938 , MCCLINTOCK 1939 , MCCLINTOCK 1941A , MCCLINTOCK 1941B , MCCLINTOCK 1942A ). From her knowledge of the behavior of broken chromosomes, she developed a method for producing small terminal and subterminal deletions (MCCLINTOCK 1942B , MCCLINTOCK 1943 ).
McClintock undertook a search for new mutations using F2 progeny derived from F1 plants that had received a recently broken chromosome 9 from one parent and the selfed progeny of plants that had received a newly broken chromosome 9 from each parent (MCCLINTOCK 1945 ). She identified a new type of chromosomal behavior in which part of chromosome 9 was lost during development. She also noted the appearance in these cultures of new variegating mutants (MCCLINTOCK 1945 ). It is clear, in retrospect, that these observations were the first emerging indications that transposable elements had been activated in her cultures. McClintock later noted that while reports of the appearance of new mutable genes were relatively rare in maize literature, she had rapidly isolated 14 new cases of such instability and observed more (MCCLINTOCK 1946 ). Continuing to examine the new type of chromosome breakage, McClintock soon understood that breakage occurred repeatedly within a restricted region or at a single site. This was supported by cytological studies that showed a chromosome 9 constitution in which one homologue lacked a large segment of the short arm. McClintock tied the two phenomena together because both variegation in the newly isolated unstable mutants and chromosome breakage showed striking differences in frequency and timing between plants, a resemblance she guessed might be more than coincidental.
By 1947 McClintock was confident enough that the chromosome breakage in the new strain was happening at a single site to name it the Dissociation or Ds locus, which she mapped both cytologically and genetically to a position near the centromere on the short arm of chromosome 9 (MCCLINTOCK 1947 ). McClintock also recognized that a second locus was required for chromosome dissociation at the Ds locus and she named it Activator or Ac, for its ability to activate chromosome breakage at the Ds locus. Turning to the investigation of the mutable loci that had surfaced in her cultures, McClintock soon realized that some were unstable only in the presence of Ac (MCCLINTOCK 1947 ). This began to provide support for her earlier guess that the chromosome breakage and mutability phenomena were related in some way.
| Ds transposition |
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It was at about this time that McClintock recognized the ability of Ds to move (MCCLINTOCK 1948 ). Her first insight came in experiments with a multiply marked short arm of chromosome 9, in which all the markers were distal to Ds and, as a consequence, were lost concomitantly after chromosome breakage. The first clue that something had changed was the observation of two exceptional kernels that did not, as expected and observed for all of the other kernels containing Ac, lose all of the dominant markers distal to Ds simultaneously. Instead, the kernels showed breaks just to the right of the I locus, giving rise to colored sectors (note that I is a dominant inhibitory allele of the C locus, required for anthocyanin pigment biosynthesis). Curiously, there were additional sectors that, in turn, had lost succeeding loci proximal to I sequentially. These observations led McClintock to an intense genetic and cytological analysis from which she concluded that the Ds element had changed its chromosomal location. McClintock also understood that, although the chromosome with the transposed Ds did not lack a telomere, Ds breaks occurring at subsequent cycles of chromosome replication could result in the joining of the two sister chromatids at the Ds insertion site. This generated a dicentric chromosome, which subsequently continued the breakage-fusion-bridge cycle, accounting for the sequential loss of markers observed in the initial odd kernels.
| Ds and mutable genes |
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Although McClintock believed that the response of Ds to Ac and the behavior of the new Ac-controlled mutable alleles were more than coincidentally similar, the relationship was not clear. McClintock's newly isolated mutations shared certain characteristics of the mutable genes studied by both Emerson and Rhoades. Particularly striking was the parallel with Rhoades' Dt-controlled mutable a1 allele (RHOADES 1938 ). The solution came when McClintock realized that the Ds element could move. This conclusion emerged from analysis of one new instance of mutability at the C locus emerging in her cultures.
The new mutable allele, designated c-m1, arose in a chromosome that carried Ds at its original position and the wild-type C allele. McClintock's crosses revealed that chromosome breakage was now closely linked to the c-m1 locus, and she formulated the hypothesis that the c-m1 allele originated by transposition of the Ds element into or near the C locus, inactivating it. To test this hypothesis, she selected 16 fully pigmented C kernels arising at a low frequency on c-m1 ears. Most of the plants grown from such kernels no longer showed evidence of Ds-type chromosome breakage. Thus, it appeared that when the c-m1 allele mutated to the wild-type C allele, all evidence of the presence of Ds disappeared (MCCLINTOCK 1948 , MCCLINTOCK 1949 ).
Thus, the last piece of the puzzle had fallen into place, explaining the basis of the variegation phenomena that had, by then, been under genetic scrutiny for almost half a century. Unstable mutations of the type analyzed by both EMERSON 1914 , EMERSON 1917 and RHOADES 1938 could be understood as the result of transposable element insertions into a locus, from which it frequently transposed during development, restoring gene function. McClintock was able to make the connection between transposition of a genetic element, the Ds locus, and the origin of a mutable gene giving a variegated phenotype, because the particular Ds element she first isolated had a second property, chromosome breakage, by which she was able to track the Ds element independently. Many of McClintock's original Ds insertion mutations were not caused by chromosome-breaking Ds elements, which have a special structure (FEDOROFF 1989 ). Nonetheless, they showed the same relationship to the Ac element as Rhoades' a1 mutation showed to the Dt locus: the mutations were unstable only in the presence of the second, activating locus. In both cases, the element inserted into the affected gene (a1, c-m1) was a transposition-defective element. Such mutations are stable because the defective element lacks an intact transposase gene. If supplied with transposase by an intact element at another chromosomal location, such an element can transpose, giving the characteristic variegated phenotype caused by frequent excision of the element from the gene during development.
Soon after, McClintock understood that Ac could itself transpose and cause insertion mutations that differed from those caused by a Ds element by being inherently unstable (MCCLINTOCK 1949 , MCCLINTOCK 1951B ). McClintock further found that the dosage of the Ac element, as well as more subtle changes in both the Ds and Ac elements, affected both the timing and frequency of chromosome breaks and transposition (MCCLINTOCK 1949 , MCCLINTOCK 1951A , MCCLINTOCK 1951B ). The Ac dosage effect is a negative one: the more copies, the greater the developmental delay in Ac-mediated breakage and transposition. Because Ac turned out to be the transposon causing pericarp variegation in Emerson's calico corn, McClintock's findings explained his puzzling observation that there is an inverse relationship between the amount of somatic reversion and the number of copies of the Pvv gene (EMERSON 1929 ).
In contemporary terms, the Ac element is a small transposon (4.5 kb) and encodes a single protein, its transposase (FEDOROFF 1989 ). Ds elements are often, although by no means always, internally deleted derivatives of an Ac element. There are many additional, structurally different transposons that are mobilized by the Ac element. Some share little sequence identity with Ac save the 11-bp terminal inverted repetitions and some subterminal transposase binding sites. By contrast, all Ac elements so far isolated are virtually identical in sequence. The chromosome-breaking Ds originally identified by McClintock has a unique structure: it consists of two short Ds elements that comprise the ends of Ac, one inserted in inverted order almost precisely into the middle of the other (FEDOROFF 1989 ). The ability of this Ds element to break chromosomes is related to its replication mechanism and the presence of both ends of the element in both orientations within its structure (ENGLISH et al. 1995 ). Deletion of part of this element can markedly change the timing and frequency of chromosome breakage without abolishing the ability of the element to transpose (FEDOROFF 1989 ). Most Ds and all Ac elements are simple in their structure and rarely or never break chromosomes.
As noted above, the element causing instability of the pericarp locus in Emerson's strains and named Mp by Brink and his colleagues is the same as Ac (BRINK and NILAN 1952 ; FEDOROFF 1989 ). Emerson's original observations that a somatic reversion event was almost always stable, except for the occasional reappearance of variegating kernels, probably find their explanation in the observation that Ac elements have a propensity to transpose to nearby sites, from which they can, once again, transpose back into the locus of origin (GREENBLATT and BRINK 1962 , GREENBLATT and BRINK 1963 ; GREENBLATT 1984 ; CHEN et al. 1992 ; MORENO et al. 1992 ). Similarly, chromosome breakage can persist after a chromosome-breaking Ds transposes away from a gene if it reinserts nearby on the same chromosome.
Rhoades had identified a different transposon family. The autonomous element of this family, Dt, mobilizes a nonautonomous 704-bp element inserted in the A1 gene to give the a1 allele (BROWN et al. 1989 ). His suggestion that "the Dt gene produces some chemical substance that accelerates the mutation rate of a1" appears prophetic in retrospect (RHOADES 1938 , p. 395). The "substance" is, of course, transposase, the transposon-encoded protein that is required for transposition and that the intact element Dt supplies to the defective element inserted in the a1 allele. Because of the nature of the mutation that he analyzed, Rhoades was able to go well beyond Emerson's insights and set the stage for McClintock. Rhoades' observation that a second gene was required for instability was very much in McClintock's awareness and important to her growing understanding of transposition as she analyzed chromosome breakage at Ds and the mutability of the c-m1 Ds insertion mutation, both of which depended on a supply of Ac-encoded transposase.
| LITERATURE CITED |
|---|
BRINK, R. A. and R. A. NILAN, 1952 The relation between light variegated and medium variegated pericarp in maize. Genetics 37:519-544[Free Full Text].
BROWN, J. J., M. G. MATTES, C. O'REILLY, and N. S. SHEPHERD, 1989 Molecular characterization of rDt, a maize transposon of the "Dotted" controlling element system. Mol. Gen. Genet. 215:239-244[Medline].
CHEN, J., I. M. GREENBLATT, and S. L. DELLAPORTA, 1992 Molecular analysis of Ac transposition and DNA replication. Genetics 130:665-676[Abstract].
CORRENS, C., 1910 Der Übergang aus dem homozygotischen in einen heterozygotischen Zustand im selben Individuum bei buntblättrigen und gestreifblühenden Mirabilis-Sippen. Ber. Dtsch. Bot. Ges. 28:418-434.
DEMEREC, M., 1928a The behavior of mutable genes, pp. 183–193 in Verhandlungen des V. internationalen Kongresses für Vererbungswissenschaft.
DEMEREC, M., 1928b Mutable characters of Drosophila virilis. I. Reddish-alpha body character. Genetics 14:359-388.
DEMEREC, M., 1929 Genetic factors stimulating mutability of the miniature-gamma wing character of Drosophila virilis.. Proc. Natl. Acad. Sci. USA 15:834-838[Free Full Text].
DEMEREC, M., 1931 Behavior of two mutable genes of Delphinium ajacis.. J. Genet. 24:179-193.
DEMEREC, M., 1935 Unstable genes. Bot. Rev. 1:233-248.
DE VRIES, H., 1905 Species and Varieties: Their Origin by Mutation. Open Court Publishing, Chicago.
EAST, E. M., and H. K. HAYES, 1911 Inheritance in Maize, Vol. 167. Bul. Conn. Agr. Expt. Sta.
EMERSON, R. A., 1914 The inheritance of a recurring somatic variation in variegated ears of maize. Am. Nat. 48:87-115.
EMERSON, R. A., 1917 Genetical studies of variegated pericarp in maize. Genetics 2:1-35.
EMERSON, R. A., 1918 A fifth pair of factors A a for aleurone color in maize and its relation to the C c and R r pairs. Cornell Univ. Agric. Exp. Stn. Mem. 16:225-289.
EMERSON, R. A., 1929 The frequency of somatic mutation in variegated pericarp of maize. Genetics 14:488-511[Free Full Text].
ENGLISH, J. J., K. HARRISON, and J. D. G. JONES, 1995 Aberrant transpositions of maize double Ds-like elements usually involve Ds ends on sister chromatids. Plant Cell 7:1235-1247[Abstract].
FEDOROFF, N., 1989 Maize transposable elements, pp. 375–411 in Mobile DNA, edited by M. HOWE and D. BERG. American Society for Microbiology, Washington, D.C.
FEDOROFF, N., 1994 Barbara McClintock (June 16, 1902–September 1, 1992). Genetics 136:1-10[Medline].
GOLDSCHMIDT, R., 1938 Physiological Genetics. McGraw-Hill, New York.
GREENBLATT, I. M., 1984 A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, Modulator, in maize. Genetics 108:471-485[Abstract/Free Full Text].
GREENBLATT, I. M. and R. A. BRINK, 1962 Twin mutations in medium variegated pericarp maize. Genetics 47:489-501[Free Full Text].
GREENBLATT, I. M. and R. A. BRINK, 1963 Transpositions of Modulator in maize into divided and undivided chromosome segments. Nature 197:412-413.
MCCLINTOCK, B., 1938 The fusion of broken ends of sister half-chromatids following chromatid breakage at meiotic anaphases. MO Agric. Exp. Stn. Res. Bull. 290:1-48.
MCCLINTOCK, B., 1939 The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc. Natl. Acad. Sci. USA 25:405-416[Free Full Text].
MCCLINTOCK, B., 1941a The association of mutants with homozygous deficiencies in Zea mays.. Genetics 26:542-571[Free Full Text].
MCCLINTOCK, B., 1941b The stability of broken ends of chromosomes in Zea mays.. Genetics 26:234-282[Free Full Text].
MCCLINTOCK, B., 1942a The fusion of broken ends of chromosomes following nuclear fusion. Proc. Natl. Acad. Sci. USA 11:458-463.
MCCLINTOCK, B., 1942b Maize genetics. Carnegie Inst. Wash. Year Book 41:181-186.
MCCLINTOCK, B., 1943 Maize genetics. Carnegie Inst. Wash. Year Book 42:148-152.
MCCLINTOCK, B., 1945 Cytogenetic studies of maize and Neurospora. Carnegie Inst. Wash. Year Book 44:108-112.
MCCLINTOCK, B., 1946 Maize genetics. Carnegie Inst. Wash. Year Book 45:176-186.
MCCLINTOCK, B., 1947 Cytogenetic studies of maize and Neurospora. Carnegie Inst. Wash. Year Book 46:146-152.
MCCLINTOCK, B., 1948 Mutable loci in maize. Carnegie Inst. Wash. Year Book 47:155-169.
MCCLINTOCK, B., 1949 Mutable loci in maize. Carnegie Inst. Wash. Year Book 48:142-154.
MCCLINTOCK, B., 1951a Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16:13-47[Medline].
MCCLINTOCK, B., 1951b Mutable loci in maize. Carnegie Inst. Wash. Year Book 50:174-181.
MORENO, M. A., J. CHEN, I. GREENBLATT, and S. L. DELLAPORTA, 1992 Reconstitutional mutagenesis of the maize P gene by short-range Ac transpositions. Genetics 131:939-956[Abstract].
PLOUGH, H. H. and C. F. HOLTHAUSEN, 1937 A case of high mutation frequency without environmental change. Am. Nat. 71:185-187.
RHOADES, M. M., 1936 The effect of varying gene dosage on aleurone colour in maize. J. Genet. 33:347-354.
RHOADES, M. M., 1938 Effect of the Dt gene on the mutability of the a1 allele in maize. Genetics 23:377-397[Free Full Text].
RHOADES, M. M., 1941 The genetic control of mutability in maize. Cold Spring Harbor Symp. Quant. Biol. 9:138-144[Abstract/Free Full Text].
SCHWARTZ, D., 1993 Marcus M. Rhoades (1903–1991). Genetics 133:1-3[Medline].
STERN, C., 1935 The behavior of unstable loci—an hypothesis. Proc. Natl. Acad. Sci. USA 21:202-208[Free Full Text].
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