The Journal of Heredity 2002:93(1)
© 2002 The American Genetic Association 93:42-47
Maize Tertiary Trisomic Stocks Derived From B-A Translocations
From the Division of Biological Sciences, University of Missouri, Columbia, MO 65211.
Address correspondence to James A. Birchler, University of Missouri, Division of Biological Sciences, 117 Tucker Hall, Columbia, MO 65211-7400, or e-mail: birchlerj{at}missouri.edu.
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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Reciprocal translocations between supernumerary B chromosomes and the basic complement of A chromosomes in maize have resulted in a powerful set of tools to manipulate the dosage of chromosomal segments. From 15 B-A reciprocal translocation stocks that have the B-A chromosome genetically marked we have developed tertiary trisomic stocks. Tertiary trisomics are 2n + 1 aneuploids where the extra chromosome is a translocation element, in this case a B-A chromosome. Whereas B-A translocations produce aneuploidy in the sperm, the tertiary trisomic plant efficiently transmits hyperploid gametes maternally. Because the B-A tertiary trisomic stocks and the B-A translocation stocks from which they were derived are introgressed into the W22 inbred line, the effects of maternally and paternally transmitted trisomic B-A chromosomes can be compared. Data are presented on both the male and female transmission rates of the B-A chromosomes in the tertiary trisomic stocks.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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B-A reciprocal translocations of maize have proven to be invaluable tools. Supernumerary B chromosomes occur only in some populations of maize (Longley 1927). Their utility derives from their tendency not to disjoin at the second pollen mitosis, resulting in one sperm receiving two copies of B and the other none (Roman 1947). This behavior was confirmed using reciprocal translocations where the B chromosomes had exchanged regions with one of the 10 A chromosomes that constitute the haploid set of maize (Roman 1947). The A segment carries a genetic marker that provides a relatively easy way to determine the presence or absence of the B-A chromosome. It was apparent from the regular noncorresponding phenotype of the embryo and endosperm that the two sperm from the same pollen grain were not identical.
The nondisjunction of the B centromere provides a means for the manipulation of the genome. Because segments are exchanged, B-A translocations result in two novel chromosomes. The A-B chromosome, that is, the centromeric portion of the A chromosome with the distal portion of the B chromosome, behaves like a proper A chromosome except that it is deficient. The B-A chromosome, that is, the centromeric portion of the B chromosome with the translocated A region, is capable of behaving like a B chromosome. The B-A chromosome can nondisjoin in the second pollen mitosis, provided that the most distal portion of the B chromosome is present in the genome (Ward 1973; Roman 1950). This means that in most cases the A-B chromosome must also be present. Nondisjunction produces one sperm that is disomic for the A segment; the other sperm is nullisomic. Depending upon which sperm fertilizes the egg, the resulting plant will be trisomic or monosomic for the translocated A region. Perhaps the most common use of B-A translocations in maize has been to determine the chromosomal location of recessive genes (Beckett 1978; Roman and Ullstrup 1951).
More recently, autonomous transposable elements have been used to increase the number of B-A chromosomes that possess genetic markers. In this way the presence of a B-A can be determined by observing the kernel phenotype (Birchler and Alfenito 1993). This has allowed comprehensive studies on the effects of chromosomal dosage on gene expression (Auger et al. 2001; Birchler 1993; Guo and Birchler 1994, 1997). This expanded collection of marked B-A translocation stocks is the starting material for the establishment of the B-A tertiary trisomic stocks.
A tertiary trisomic is a 2n + 1 aneuploid where the extra chromosome is a translocation chromosome, in this case a B-A translocation. They can be used for chromosomal dosage studies in a manner similar to B-A reciprocal translocations. Although trisomic plants segregate for only two genetic conditions, euploidy and hyperploidy, the system is simpler to use than B-A translocations. Here we describe this new collection of B-A tertiary trisomic stocks, how they were produced, and how they are manipulated. In addition, data are presented on both the male and female transmission rates of the B-A chromosomes.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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The starting materials for this project were 15 B-A translocation stocks where the B-A chromosomes are marked with dominant genetic markers. These markers allow the presence of the B-A chromosome to be detected by observing the phenotype of the embryo and endosperm (Birchler and Alfenito 1993; Birchler and Guo 1997). Of the B-A translocation stocks used, this is the first report of a marked TB-3Sb stock. Its B-A chromosome was recombined with a chromosome possessing an Activator (Ac) transposable element (trAc8163; Dooner et al. 1994). All 15 B-A stocks and their testers have been introgressed into the W22 inbred line.
Plants possessing the various B-A translocations were crossed as males onto appropriate testers. Due to nondisjunction of the B-A chromosome at the second pollen mitosis, many of the progeny had embryos that were disomic for the B-A chromosome and therefore were hyperploid for the translocated A chromosomal arm. Kernels with hyperploid embryos were selected, grown, and crossed as females again by the appropriate tester stocks (Figure 1). The progenies of these crosses were expected to segregate approximately 1:1 for euploids and tertiary trisomics. Samples of kernels were selected and grown from each of the B-A stocks. The resulting plants were crossed reciprocally with the appropriate tester stock. Balanced euploids were distinguished from trisomic plants by the rate and manner of transmission of the color markers through the pollen. We expected that trisomic plants would show reduced transmission of the genetic marker when crossed as the male onto a tester plant because aneuploid pollen does not compete well with euploid pollen (McClintock and Hill 1931; Rhoades 1933). In addition, the embryo and endosperm of each kernel resulting from such a cross should consistently show correspondence of color phenotype because the A-B chromosome is absent (Figure 1).
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Ears were harvested from plants that appeared to be trisomic for the B-A chromosome. Colored (or spotted) kernels were selected for testing in a subsequent generation. Again these kernels were grown and crossed reciprocally with an appropriate tester stock. Both the male and female transmission frequencies of the genetic marker were recorded for the putative trisomic plants. From the resulting progeny of these reciprocal crosses, a small sample of kernels was selected for germination and root tips were harvested to determine the karyotype. Chromosome slide preparations were performed according to the method developed by Kato (1997, 1999). Root tips were treated with pressurized nitrous oxide (10 atm) for 1.5 h and then fixed in cold 90% acetic acid for 10 min. After rinsing the roots in tap water, the tips were excised using a razor blade and digested in a mixture of 1% pectolyase Y-23 and 2% cellulase Onozuka R-10 (Yakult Honsha Co., Tokyo) for 80 min at 37°C. The macerated tissues were spread on microscope slides with a 1:1 mixture of ethanol and glacial acetic acid. Chromosomes were stained with acetic orcein.
Some plants possessed one or more B chromosomes in addition to the B-A chromosomes. Usually there were sufficient morphological differences between the B and B-A chromosomes to allow them to be distinguished. When the B-A chromosome could not be reliably distinguished from the B chromosome by morphology, fluorescence in situ hybridization (FISH) was performed using the B-specific probe. The B-specific probe was derived from a 1.4 kb fragment that was cloned into pBS KS+ (Stratagene, La Jolla, CA) (Alfenito and Birchler 1993). The B-specific fragment was amplified via polymerase chain reaction (PCR) and labeled with digoxigenin-11-dUTP using nick translation. One-ninth volume 20x SSC was added to the probe solution after the nick translation reaction and the resulting mixture was used directly for hybridization. To each slide 3 µl of the mixture was added and a 22 mm x 22 mm plastic coverslip was applied. The slides were placed in an aluminum tray and floated in a larger vessel of covered boiling water for 5 min in order to denature the probe and the target DNA. The slides were transferred to a sealed container for overnight hybridization at 37°C. A paper towel moistened with 2x SSC was added to prevent drying. After hybridization, the slides were washed in 2x SSC at room temperature for 5 min with gentle agitation, then in 2x SSC at 55°C for 15 min and then in 1x PI buffer at room temperature for 5 min. PI buffer consisted of 0.2 M NaH2PO4 and 0.1% Igepal CA-630 (Sigma, St. Louis, MO) at pH 7.8. The slides were drained but not dried and a 50 µl solution of Cy3-conjugated IgG fraction monoclonal mouse antidigoxigenin antibody (Jackson ImmunoResearch Laboratories, West Grove, PA) diluted 1:100 in a PI buffer containing 3% BSA (Sigma A-9647) was applied. A slip of parafilm (approximately 22 mm x 22 mm; American National Can, Neenah, WI) was placed on each slide, which was subsequently incubated at 37°C for 1 h in a humid container. The slides were washed in PI buffer at room temperature. A drop of mounting medium (Vectashield, Vector Laboratories, Burlingame, CA) with 1.5 µg/ml 4', 6-diamidino-2-phenylindole dihydrochloride (DAPI) and a coverslip were applied to each slide prior to microscopic observation. B chromosomes were readily identifiable due to characteristic signals at the centromere and near the tip of the chromosome (Alfenito and Birchler 1993).
For RNA analysis of dosage, samples of approximately 20 euploid and 20 trisomic 6Lc embryos were harvested 30 days after pollination and immediately frozen at -80°C. RNA extraction and quantitative northern analysis were performed exactly as described in Auger et al. (2001). Probes were used to identify transcripts from genes that encode cytochrome c oxidase subunit 1 (cox1; Kuzmin E, unpublished data), cytochrome c oxidase subunit 3 (cox3; Hiesel et al. 1987), cytochrome oxidase subunit Vb (cox5b; Pioneer HiBred Int., unpublished data), ATP synthase alpha subunit (atpA; Mulligan et al. 1988), and 18S mitochondrial rRNA (rrn18; Mulligan et al. 1988).
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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Tertiary trisomies were identified for each of the B-A chromosomes (Table 1). Stocks are designated according to the original B-A chromosome that is responsible for the segmental trisomic condition. For example, the stock derived from the TB-1Sb translocation is designated triB-1Sb. TB-1Sb involves the exchange of a portion of the B chromosome with the short arm of chromosome 1. The suffix, b, is given to differentiate this B-A from any others that may involve the same two chromosomes but that have different breakpoints. The breakpoint of the A chromosome describes the cytological position as a proportion of the particular A chromosome arm in question. For triB-1Sb the breakpoint is at 0.05, that is, the distal 95% of the short arm of chromosome 1 is on the B-A chromosome. The B-A marker indicates the dominant gene or autonomous transposable element that is used to mark genetically the presence or absence of the B-A chromosome in the mature kernel. Except where noted, all stocks have dominant color alleles for a1, a2, c1, c2, bz1, bz2, pr1, and r1. The appropriate tester for each trisomic stock is a euploid that possesses the tester allele, but otherwise has all of the dominant genes listed previously that condition kernel color. A general description of each B-A chromosome is given in Table 1.
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Transmission of B-A Chromosomes in Tertiary Trisomics |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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We expected that transmission of the B-A marker through the male gamete from trisomic plants would be reduced and that this would serve to identify these tertiary trisomics. The generally accepted explanation for this phenomenon is that aneuploid pollen fail to compete with euploid pollen in pollen tube growth (Buchholz and Blakeslee 1932). The transmission rate of the B-A marker through both the female and male gametes is illustrated in Figure 2. Except for triB-3Sb, triB-9Lc, and triB-10L19, male transmission of the marker was substantially reduced from a theoretical maximum of 50%. Also remarkable was the substantial reduction in female transmission of the markers for triB-4Sa, triB-5Sc, and triB-7Lb. The reduction in the marker transmission rate can be used to confirm that an individual plant is trisomic. Because female transmission of the B-A chromosome is more efficient, it is the preferred method of propagating these stocks.
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The transmission of the marker from the male can be due to transmission of the B-A chromosome or to the crossover of the marker onto the respective A chromosome. For each trisomic stock, chromosome counts were made of a small sample of female and male progeny that possessed the markers. The marker transmission rates and cytology data were used to estimate the rates of B-A transmission (Table 2). The B-A transmission rate is the product of the marker transmission rate and the proportion of the marked kernels that possessed a B-A chromosome.
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Most individuals in which the marker is present but not the B-A chromosome result from the crossover of the marker from the B-A chromosome to a normal A chromosome in the parent. Although transposable element markers may move from the B-A chromosome without crossover, it is unlikely that such events contribute significantly to classification error. Most of the transposable elements used as markers tend to transpose late in development, and transposed elements are rarely transmitted germinally (Dempsey 1993; Rhoades 1938). The element most likely to do so is Ac (Activator) and in this case the great majority of the transposed Acs are on the same chromosome (Van Schaik and Brink 1959). Confirmation of trisomy can be made by evaluating the results of reciprocal crosses with the appropriate tester, cytological examination, molecular polymorphisms, and in many cases phenotypic characteristics (e.g., shorter stature and delayed anthesis of the trisomic plant).
The reduced rates of B-A transmission through the pollen (Table 2) are consistent with the idea that the effects of aneuploidy are due to individual dosage-dependent factors that are distributed throughout the genome (Birchler and Newton 1981; Guo and Birchler 1994). When the vegetative cell of a pollen grain possesses an extra chromosomal segment that possesses one of these factors, its ability to mediate pollen tube growth is inhibited. Ostensibly this is due to the dosage-dependent factor down-regulating some rate-limiting function. Longer chromosomal segments are more likely to possess such a factor but this relationship is not absolute. Although the A segment of B-10L19 is cytologically longer than the A segment of B-4Sa, the former displays little reduction in transmission through the pollen, while the latter is profoundly reduced. The high male transmission rate of B-10L19 indicates that it possesses few dosage-dependent genes that affect pollen transmission. This also appears to be true for B-3Sb.
Nearly all of the B-A chromosomes show some reduced female transmission (Table 2). Note that several B-As suffered a nearly 50% loss in female transmission rate. Of interest, the female transmission rates correlate with the size of the B segment and not the size of the A segment. The B chromosome is a nearly telocentric chromosome whose long arm is characterized as having four main parts: a small proximal heterochromatic knob, a proximal euchromatic region, a large distal heterochromatic region, and a small distal euchromatic tip (Randolph 1941; Ward 1973; Figure 3). All of the B-As that are known to have breakpoints in the proximal euchromatic region (B-1La, B-4Sa, B-7Lb, and B-9Lc; Table 1) have estimated female transmission rates of less than 30% (average 25.6%; Table 2). The other known B breakpoints are in the distal heterochromatic region (B-1Sb, B-3Sb, B-3La, B-4Lb, B-6Lc, B-9Sd, and B-10L19; Table 1). All of these B-As have estimated transmission rates of more than 30% (average 35.5%; Table 2). It appears that there are factors in the distal heterochromatic region that prevent B loss. Carlson and Roseman (1992) found that several deletions in the B component of TB-9Sb resulted in meiotic loss of the B-A chromosome. One deletion that had an effect was in the distal heterochromatin.
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A tertiary trisomy that is not part of the basic set, triB-10L32, underscores the observation that the reduction in B-A male and female transmission rates occurs by different mechanisms. TriB-10L32 was generated from TB-10L32 in the same manner as the others. It differs from triB-10L19 in that its A breakpoint is 0.74 on the long arm of chromosome 10 (Maguire 1985). While the male transmission rate for B-10L32 is hardly reduced, the female transmission rate is reduced dramatically (Figure 4). The B breakpoint for B-10L32 has not been described, but it appears to be quite proximal, because cytological observation of mitotic root-tip cells reveals that it is the smallest of all the B-As examined in this study.
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RNA Expression: TriB-6Lc versus TB-6Lc |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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The tertiary trisomic B-A stocks were developed as additional tools to analyze the effects of segmental chromosomal dosage. They complement the B-A reciprocal translocation stocks in that the effect of a maternally inherited B-A chromosome can be compared to the effects of the same B-A chromosome inherited paternally. On a gross phenotypic level, the tertiary trisomic plants, which received a B-A chromosome maternally, resemble the plants that are trisomic because they received two B-A chromosomes paternally due to nondisjunction in the second pollen mitosis. This is particularly notable for the prominent trisomic syndromes. For example, regardless of whether the B-A chromosome is inherited maternally or paternally, trisomic 1La plants are stocky and consistently have delayed anthesis; trisomic 5Sc plants have leaves that are short and wide; and trisomic 7Lb plants have anthers that dehisce poorly.
In a recent study (Auger et al. 2001), the dosage effects that paternally generated B-A dosage series had upon the mRNA levels of several mitochondrial genes were documented. In a similar fashion, the steady-state RNA levels were determined for triB-6Lc. Data are given for mRNA expression levels of four mitochondrial genes (cox1, cox3, atpA, and rrn18) and one nuclear gene that encodes a mitochondrial component (cox5b) (Table 3). Expression levels for tertiary trisomic embryos are listed as maternal and expression levels from the previous study (Auger et al. 2001) are listed as paternal. The RNA levels are given as proportions of the euploid expression level (i.e., euploid = 1.00) for each gene. Asterisks indicate that the aneuploid expression level was significantly different from the euploid (t test, P < .05). In one case, atpA, the effect of the maternally inherited B-A chromosome differed from the paternal (Table 3). It is possible that this difference was due to parental imprinting. Alternatively, because the B-A tertiary trisomic stocks and the B-A translocation stocks were not fully isogenic, it is possible that the difference in 6Lc dosage effect upon atpA was due to allele-specific factors. Generally the molecular effects of trisomy do not appear to be sensitive to the mode of transmission of the trisomic segment.
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Further Uses |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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B-A tertiary trisomics can be used to maintain lethal or deleterious genes (Beckett 1991). In an otherwise homozygous plant, the trisomic B-A chromosome will complement a recessive trait. Further, because the B-A transmission rate is reduced, the percentage of gametes that possess the uncomplemented recessive allele is increased. For example, a tertiary trisomic stock could be developed that is otherwise homozygous for a lethal recessive mutation. At least one-half of the eggs from such a plant will carry the uncomplemented mutant allele. Nearly all successful pollen will carry the mutation. It can be expected that less than one-half of the kernels on a self-pollinated ear from such a plant would have the nonmutant phenotype and nearly all of those will be trisomic. By comparison, three quarters of the kernels from a self-pollinated ear of a heterozygous plant without the extra chromosome are expected to be nonmutant and one-third of those will be homozygous +/+.
There is the potential for the B centromere to suffer misdivision in meiosis, which may result in useful chromosomal aberrations (Carlson 1970). The tertiary trisomic stocks could be used to generate isochromosomes of the respective B-As, which would duplicate the chromosome arm involved. Individuals bearing such chromosomes would be tetrasomic for the A segment. Tetrasomy could also be achieved by crossing the B-A trisomic plant as a female with pollen from a homologous B-A translocation plant. The tertiary trisomic plant produces eggs with one or two copies of the A segment; the B-A translocation produces sperm with zero, one, or two copies of the A segment. If alternative markers can be identified so that a maternally derived B-A chromosome can be distinguished from a paternally derived B-A chromosome, then a B-A dosage series with one to four A segments could be identified. Alternatively, the dosage series could be classified by cytological examination.
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Acknowledgments |
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The procedure for fluorescence in situ hybridization outlined in the methods section was developed by A. Kato. The starting genetic materials were provided by the Maize Genetics Cooperation Stock Center, M. Rhoades, E. Dempsey, M. Alleman, J. Beckett, H. Dooner, S. Dellaporta, N. Fedoroff, and M. Alfenito. The DNA clones used in this study were provided by R. Hiesel, E. Kuzmin, M. Mulligan, and Pioneer HiBred International. We thank A. Kato for his critical reading and comments and C. Ostlie, who reviewed the manuscript for grammatical and other errors. The described stocks will be sent to the Maize Genetics Cooperation Stock Center (S-123 Turner Hall, 1102 South Goodwin Ave., Urbana, IL 61801-4798) upon publication. This research was supported by a grant from the Department of Energy Biosciences Program.
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Footnotes |
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Corresponding Editor: J. Perry Gustafson
Received June 29, 2001
Accepted November 26, 2001
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionTransmission of B-A Chromosomes...RNA Expression: TriB-6Lc versus...Further UsesReferences |
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