Analysis of Nondisjunction Induced by the r-xi Deficiency During Microsporogenesis in Zea mays L.
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1 Copyright 988 by the Genetics Society of America Analysis of Nondisjunction Induced by the r-xi Deficiency During Microsporogenesis in Zea mays L. Zuo-Yu Zhao' and David F. Weber Department of Biological Sciences, Illinois State University, Normal, Illinois 6 76 Manuscript received January 8, 988 Accepted April 6, 988 ABSTRACT The r-x deficiency in maize induces nondisjunction at the second mitotic division during embryo sac formation. However, it was not known if this deficiency also induces nondisjunction during the microspore divisions. Microsporogenesis in plants lacking or containing this deficiency was compared usingtwoapproaches.first,chromosomenumbersweredeterminedingenerativenuclei.many (8.%) of the generative nuclein r-xi-containing plants were aneuploid; however, those from control plants were all haploid. Thus, this deficiency induces nondisjunction during the first microspore division. Second, nucleoli were analyzed in microspores. The only nucleolar organizing region in maize is on chromosome 6. If chromosome 6 underwent nondisjunction during the first microspore division, one nucleus in binucleate microspores would contain no nucleolus and the other would contain two nucleoli (or one nucleolus if the nucleoli fused). Only one (.%) microspore of this type was observed in control plants while.% were found in r-xi-containing plants. Thus, the r-x deficiency induces nondisjunction of chromosome 6 during the first microspore division. However, both of the sperm nuclei in trinucleate microspores contained one nucleolus in r-xl-containing and control plants; thus, this deficiency does not induce nondisjunction of chromosome 6 (and presumably other chromosomes) during the second microspore division. HE r-xi deficiency in maize is a submicroscopic T deficiency including the R locus on chromosome, which was induced with X-irradiation by L. J. STADLER (unpublished data). K. SATYANARAYANA (unpublished data) found that plants carrying this deficiency crossed as female parents produced large numbers of monosomic and trisomic progeny. s monosomic for nine, possibly for all ten of the maize chromosomes have been generated by this deficiency, and these monosomic plants have been utilized in numerous studies (reviewed in WEBER 98, 986; HELENTJARIS, WEBER and WRIGHT 986). R/r-XI plants testcrossed as female parents produce 55-6% colored (R/r) kernels and colorless (r/r-xl) deficiency-containing kernels. s germinated from the R/r kernels are invariably diploid, whereas those germinated from r/r-xl kernels include - 8% monosomics and - 8% trisomics as well as a low frequency of multiple aneuploid plants. The remaining plants are diploid (WEBER 98). Because approximately equal frequencies of monosomics and trisomics are generated by this deficiency, the generation of aneuploids appears to be due to nondisjunction. Studies have been carried out to identify the division(s) at which the r-xi deficiency induces nondisjunction. Nondisjunction does not appear to occur ' Present address: Cold Spring Harbor Laboratory, P.O. Box, Cold Spring Harbor, New York 74. during meiosis in r-xi-containing plants because meiosis appears to be normal in these plants (D. F. WEBER unpublished data). Also, a single nucleolus is present in each of the four haploid microspores of quartets of these plants (D. F. WEBER 978 and unpublished data). A single nucleolar organizing region (NOR), which is located on chromosome 6 (Mc- CLINTOCK 94), is present in the maize genome. If chromosome 6 underwent nondisjunction at the first meiotic division, two of the four members of the resultant quartet would contain two chromosome 6s (and two nucleoli) and two would contain none. If chromosome 6 underwent nondisjunction at the second meiotic division, two would contain one, one would contain two, and one would contain no nucleolus (WEBER 98). Because each of the four members of each quartet contains a single nucleolus, chromosome 6 (and presumably the other chromosomes) does not undergo nondisjunction during either meiotic division. Thus, nondisjunction induced by the r-xi deficiency occurs after meiosis is completed. To determine if the r-xi deficiency induces nondisjunction during the megagametophyte divisions, male parents with closely linked recessive seedling and seed mutations were crossed to females carrying the r-x deficiency and dominant alleles of the linked mutations (WEBER 98). Progeny expressing the recessive seedling mutation (monosomic for the chromosome carrying the dominant alleles) had not lost the domi- Genetics 9: (August, 988)
2 976 Zhao Z.-Y. and D. F. Weber nant allele of the seed mutation in their endosperms. Thus, there was a noncorrespondence between the genetic constitutions of the embryo and endosperm of kernels containing monosomic embryos. This indicated that the nondisjunction that produced the monosomic must have occurred after meiosis during one or more of the embryo sac mitotic divisions. Two recent studies have indicated that the r-x deficiency induces nondisjunction at the second mitotic division during embryo sac formation. LIN and COE (986) analyzed chromosome numbers in r-xicontaining kernels of different sizes. Their work was based on the largely untested assumption that an extra or missing copy of any of the maize chromosomes would significantly reduce the size of the endosperm. They obtained results that are consistent with the assumption that nondisjunction takes place at the second mitosis during megasporogenesis. SIMCOX, SHAD- LEY and WEBER (987) determined the number of maternally-contributed chromosome 6s in endosperms of kernels containing monosomic-6 embryos. Normal endosperms are triploid and contain two maternally contributed copies of each of the chromosomes. Five kernels with monosomic-6 embryos were recovered, and each of these kernels contained only one maternally contributed chromosome 6 in its endosperm. Such a kernel could only be formed if nondisjunction occurred at the second megaspore division. Furthermore, the data suggest that the polar nucleus contributed by the micropylar end and the egg nucleus are sister nuclei. These studies indicate that nondisjunction induced by the r-x deficiency occurs at the second megagametophyte division. However, the data do not preclude the possibility that nondisjunction also occurs at the first and/or third division at a much lower frequency. R/r-X plants testcrossed as male parents produce only colored (Rlr) kernels; thus, pollen grains containing the r-x deficiency do not function. This is surprising because these plants have normal appearing pollen; thus, pollen grains containing this deficiency do not function even though they appear to be morphologically normal. s germinated from these R/ r kernels are invariably diploid. The purpose of the current study was to determine if the r-x deficiency also induces nondisjunction in microspores; and if it does, to determine the division+) at which it occurs. Because pollen grains containing the deficiency do not function, it is not possible to analyze r-x-containing progeny of plants crossed as male parents to determine if nondisjunction had taken place. To answer this question, the microspore divisions have been analyzed cytologically. The present study indicates that the r-x deficiency causes nondisjunction during microsporogenesis, and that the nondisjunction occurs during the first microspore mitosis but not during the second microspore mitosis. MATERIALS AND METHODS Genetic stocks: An R/r-XI stock in the inbred W and Mangelsdorfs multiple chromosome tester (which is r/r) were generously provided by K. SATYANARAYANA, University of Wisconsin. An R/R stock in the inbred W was originally obtained from J. KERMICLE, University of Wisconsin. These lines have been maintained for many years by D. F. WEBER. Treatment of materials: Root-tips were analyzed from each plant utilized in this study to be certain that it was a diploid. They were pretreated hr in.% 8-hydroxyquinoline at room temperature, fixed in three parts 95% ethyl acohol:one part glacial acetic acid, and kept at -". They were stained using procedures described by ZHAO and Gu (988). Immature tassels for analysis of microspore divisions were collected when -5 cm of the tassel was visible above the leaf whorl. They were treated at " for 4 hr in a moist chamber to break down the spindle, transferred into a 4: mixture of 7% ethyl alcohol:formaldehyde, kept at -" and analyzed as described by KINDICER and BECKETT (985). Three plants of each type were analyzed. One of the plants of each type analyzed was grown during one summer and the other two were grown during a different summer. Statistical methods: The data were analyzed by contin- gency x' procedures to determine whether significant differences exist among plant types. Data from three plants of each type were compared for homogeneity, and if no significant differences were found, data from the three plants were pooled and used to represent the plant type. Comparisons have been made between RIr-XI and R/R, between r/ r-xi and R/r, between R/r-XI and?-/?+-xi, and between R/ R and R/r plants. RESULTS Analysis of chromosome numbers in generative nuclei: Each microspore in a normal maize plant contains ten chromosomes, and it undergoes two mitotic divisions during the formation of a mature trinucleate pollen grain. The first division is asymmetric, producing a relatively large vegetative nucleus and a smaller generative nucleus. The generative nucleus divides during the second microspore division to produce two sperm nuclei; however, the vegetative nucleus does not divide. If nondisjunction occurred during the first microspore division, nine or chromosomes would be present at mitosis of the generative nucleus during the second microspore division. Thus, it is possible to determine whether nondisjunction takes place during the first microspore division by analyzing mitosis at the second microspore division. R/r-X plants were crossed as female parents with R/R males, and FI sibling diploid R/R and RIr-X plants were analyzed. Both parents were in the same inbred genetic background, W. Thus, the two types of progeny were nearly isogenic. Chromosome numbers were determined in the dividing generative nucleus at late prophase or metaphase during the second
3 Nondisjunction in r-x Microspores 977 TABLE Chromosome numbers atlate prophaseor metaphase in generative nuclei Chromosome in dividing generative nucleus type R/R Rh-X Rlr r/r-xl b S(.6) 4 (.8) 5(.7) (.) IO 7()" () 85() 54() I 8(94.8) 7 (.6) 5 (9.) 6(4.) lss(88.6) 4(7.6) 48 (9.) 7 (5.) (.) (.4) 45() 8() () 94() # - n b (.5) 64 (94.) (4.4) 5 (.) 47 (89.) (7.9) 4 (4.4) 8 (9.) (.) (.) 94(9.) 9 (5.9) a Numbers in parentheses are percent. The frequency of aneuploid cell types in the total was significantly different (P<.) from the frequency in sibling plants lacking the deficiency, but was not significantly different (P>.5) between the two deficiency-containing types. microspore mitosis. Three plants of each type were analyzed (Table ). Each of the 5 4 nuclei from R/R plants contained ten chromosomes; however, of the 5 nuclei from R/r-XI plants contained nine chromosomes, 7 contained, and two contained. Cells of each of these types are shown in Figure. R/r-XI plants in the inbred W genetic background were alsocrossed by an unrelated inbred, MANCELSDORF'S multiple chromosome tester, which is r/r. Three R/r and three r/r-xl sibling FI progeny of this crosswere analyzed (Table ). These plants are also nearly isogenic because they are progeny of a cross between two highlyinbred parents. At late prophase or metaphase of the second microspore division, all 94 nuclei from R / r plants were haploid whereas ten of the nuclei from r/r-xl plants contained nine chromosomesand 9 contained. Clearly, nondisjunctiontakesplace during the first microspore division in plants with the r-xi deficiency, and nondisjunction was not found in plants which lacked this deficiency. Thus, the r-xi deficiency induces nondisjunction at the first microspore division. Analysis of nucleoli at the binucleate stage: The NOR is the portion of the genome that is responsible for the formation of a nucleolus. In maize, a single NOR resides on chromosome 6 (MCCLINTOCK 94); thus, each euploid microspore nucleus contains one chromosome 6 (and one nucleolus).disjunctionof chromosome 6s can readily be followed by analyzing nucleoliin daughter cells,as described by WEBER FIGURE.-Microspores in r-xltontaining plants at the second microspore division. (A) A microspore at metaphase with ten chromosomes in the generative nucleus, (B) a microspore at metaphase with chromosomes in the generative nucleus, (C) a microspore at metaphase with nine chromosomes in the generative nucleus, and (D) a microspore at late-prophase with chromosomes in the generative nucleus. Size bar = 8 pm. ( 98 ). If chromosome6 disjoins normallyat the first microspore mitosis, daughter vegetative and generative nuclei of microspores would both contain one chromosome 6 (and one nucleolus) (Figure A). However, if chromosome 6 undergoes nondisjunction, the nucleus that receives no chromosome 6 has no NOR and the nucleus with two chromosome 6s hastwo NORs. Cells containing two NORs usually contain a single nucleolus because nucleoli frequently fuse with each other. Binucleatemicrospores produced by siblingr/r and R/r-X plants and sibling R/r and r/r-xl plants from the crosses described in the previoussection were analyzed. The data are presented in Table. Only one (.%) binucleate microspore of the type expected if nondisjunction of chromosome 6 took place at the first microspore division was found in plantslacking the r-xi deficiency;however,.% were of this type in r-xi-containing plants. Each of the exceptional microspores had no nucleolus in one nucleus and onenucleolus inthe othernucleus (Figure, B-D); no cells withno nucleolus in one nucleus and two in the other one were observed. This result also indicates that nondisjunction of chromosome 6 (and presumably other chromosomes) is induced by the r-
4 Zhao 978 I,. Z.-Y. and D. F. Weber fip,, - '/..a, / bl ('. y: TABLE Numbers of nucleoli in vegetative and generative interphase nuclei type R/R '. 8 R/r-XI l(o.9) C D R/r +e r/r-xi of microspores with: I-VN'/l-CN' I-VN/O-GN' -VN'/I-GN 6 6 ()' (99.7) () (.) 9 (99.9) (.8) A 4 88 (97.) 5 (.5) (.75) 7 S(.97) 58 5(98.84) (99.79) (. ) Totav (98.9) (.54) (.54) () () () () 4 45 (98.8) (.95) (98.6) (99.6) 4 ' (98.86) (.47) (.67) (.67) (.4) (.7) 5 (.7) 7 (.47) ' -VN = one nucleolus in vegetative nucleus. * -GN = one nucleolus in generative nucleus. FIGURE.-Binucleate microspores in the r-xlcontaining plants. (A) A normal microspore with one nucleolus in the vegetative nucleus and one in the generative nucleus (-VN/l-GN), (B)a microspore immediately after the first microspore mitosis with one nucleolus in the vegetative nucleus and none in the generative nucleus (-VN/O-GN), (C)a microspore with no nucleolus in the vegetative nucleus and one in the generative nucleus (-VN/l-GN), and (D)a microspore with one nucleolus in the vegetative nucleus and none in the generative nucleus (-VN/O-GN) (V = vegetative nucleus, G = generative nucleus). Size bar = Cm. X I deficiency at the first microspore division; however, loss of chromosome 6 from one of the two nuclei wouldalso produce thissame result. Thus, results from these two different experimental approaches are in agreement, and indicate that the r-xi deficiency induces nondisjunction during the first microspore division in maize. Analysis of nucleoli at the trinucleatestage!: The number of nucleoli inthe sperm nuclei of trinucleate microspores was analyzed to determine if nondisjunction of chromosome 6 takes place during the second microspore division. If chromosome 6 disjoins normally at the second microspore division, both sperm nuclei in the resultant trinucleate microspore would contain one chromosome 6 (and one nucleolus). However, if nondisjunction of chromosome 6 takes place during thesecond microspore division, one of the two sperm nuclei would contain no NOR (and no nucleolus) and the other one would contain two NORs (and or nucleoli for reasons discussed previously).the number of nucleoli in sperm nuclei was determined in each of the previously described plants: exactlyone nucleolus was observed in each sperm nucleus for 9 '-GN = no nucleolus in generative nucleus. d -VN = no nucleolus in vegetative nucleus. ' Numbers in parentheses are percent. 'The data from -VN/O-GN and -VN/l-GN are combined prior to comparing. The frequency of microspores with aneuploid nuclei (including -VN/O-GN and -VN/l-GN) was significantly different (P<.) from the frequency in sibling plants lacking the deficiency, but was not significantly different between the two deficiencycontaining types. nuclei from three R / R plants, 64 from three R/r-XI plants, 664 from three R/r plants and 84 from three r/r-xi plants. The microspore type expected if chromosome 6 underwent nondisjunction during the second microspore divisionwas not found in any of these plants. We concludethat the r-xi deficiency does not induce nondisjunction ofchromosome 6 (and presumably other chromosomes) during the second microspore division. However,it is possible that microspores which underwent nondisjunction during the second microspore division do not survive until the trinucleate stage. This possibility is considered to be extremely unlikely because() the vegetative nucleus of such a cell wouldbe euploid and most ofthe metabolic activity takes place in this nucleus, and () this cell type would be found immediately after the second microspore division was completed. In fact, cells nullisomic for chromosome 6 are able to complete the second meiotic division (WEBER 978) and the first microspore division (ZHAOand WEBER988). Also, the current study shows that cells which underwent nondisjunction of chromosome 6 or other chromosomes are able to complete the first microspore division and survive untilthe binucleate stage.
5 DISCUSSION The current study indicates that the r-xi deficiency induces nondisjunction during the first, but not during the second division during microsporogenesis. Recent studies by LIN and COE (986) and SIMCOX, SHADLEY and WEBER (987) indicate that nondisjunction in r-xl-containing embryo sacs occurs primarily, if not exclusively at only one of the three embryo sac divisions (the second division). Thus, the r-xi deficiency appears to induce nondisjunction at a single division during microsporogenesis and at a single division during megasporogenesis. However, it induces nondisjunction during the first division during microsporogenesis and the second division during megasporogenesis. These observations could imply that the first division of microsporogenesis is related in some way to the second division of megasporogenesis because they are affected in a similar way by the r-xi deficiency at this specific stage. When R/r-XI plants in the inbred W were crossed as female parents, 9.9% of the r-x-containing progeny were monosornics (WEBER 986). The frequency of monosornics produced by this cross may be an underestimate of the frequency of embryo sacs with n - eggs because some of the embryo sacs containing n - eggs may not produce viable kernels or because kernels containing monosomic embryos may not germinate as readily as those from n eggs. Microspores in r-xi-containing plants were also analyzed in the current study;.6% of these microspores contained hypoploid generative nuclei. Nondisjunction only appears to occur in r-xi-containing microspores, and half of the microspores in these plants contain the r-xi deficiency. Thus,.6% X or 5.% of r-x-containing microspores have hypoploid generative nuclei. This frequency (5.%) is somewhat less than the frequency of hypoploid progeny recovered when plants containing this deficiency were crossed as female parents (9.9%). However, the frequency of hyperploid generative nuclei (also produced by nondisjunction) is 5.7%; thus, the frequency of hyperploid generative nuclei in r-xi-containing microspores is 5.7% X or.4%, a value quite similar to the 9.9% monosomic progeny. The frequency of hyperploid generative nuclei may be a more reliable estimate of the frequency of nondisjunction during the first microspore division than the frequency of hypoploid nuclei because nuclei hypoploid for specific chromosomes might not be able to survive until the second microspore mitosis. Thus, the r-xi deficiency induces nondisjunction primarily, if not exclusively, at a single division in microspores and megaspores, and the frequency of aneuploid cells produced is similar. r-xi-containing plants were also analyzed at the binucleate stage of microsporogenesis;.6% of the microspores lacked a nucleolus in the generative nu- Nondisjunction in r-x Microspores 979 cleus and.5% lacked a nucleolus in the vegetative nucleus. Microspores of these types would be produced if chromosome 6 underwent nondisjunction at the first microspore division. Because these two types of microspores were found in essentially equal frequencies, it appears that both nondisjunctive types have similar survival frequencies. If each of the ten maize chromosomes underwent nondisjunction at this frequency (average.56%),.56% X or 5.6% of the microspores at the second mitotic division would have hyperploid generative nuclei and 5.6% would have hypoploid generative nuclei. Frequencies similar to this expectation (.6% and 5.7%) were indeed found; thus, chromosome 6 appears to undergo nondisjunction at a rate that is similar to the average rate of nondisjunction of the other chromosomes. Also, because about half of the microspores contain the r- XI deficiency and.6% of the generative nuclei lacked a nucleolus,.6% X or.% of the generative nuclei in microspores would be nullisomic for chromosome 6. The frequency of monosomicd plants recovered in r-xi-containing progeny of W RIr-XI females is.89% (WEBER 986). Thus, the frequency of generative nuclei nullisomic for chromosome 6 is similar to, but somewhat lower than, the frequency of monosomicd progeny recovered in r-xl-containing kernels of this same plant type crossed as a female parent. It was previously mentioned that binucleate microspores that did not contain a nucleolus in their gen- erative nuclei (nullisomic for chromosome 6) were observed. If these generative nuclei that were nullisomic for chromosome 6 were able to complete the second microspore division, trinucleate microspores would be produced which lack nucleoli in both of their sperm nuclei. No trinucleate microspores of this type were found; therefore, it appears that generative nuclei nullisomic for chromosome 6 do not survive to complete the second microspore division. Twenty-two hypoploid and 48 hyperploid generative nuclei were observed in this study in r-xl-contain- ing plants at the second microspore mitosis. This ratio is significantly different (P <. ) from a ratio of : as determined by a x* test; therefore, significantly fewer hypoploid generative nuclei than hyperploid generative nuclei were observed. One explanation for this is that some of the hypoploid generative nuclei do not survive to the second microspore mitosis. However, hypoploid mitotic nuclei were observed in this study at the second microspore mitosis, and this indicates that generative nuclei hypoploid for at least some of the maize chromosomes reach this stage. One must keep in mind that microspores with hyperploid generative nuclei contain hypoploid vegetative nuclei, and microspores with hypoploid generative nuclei contain hyperploid vegetative nuclei. Because the vegetative
6 98 Z.-Y. Zhao and D. F. Weber nucleus controls the development of the microspore in the male gametophyte, it would seem most likely that microspores of the former type would be more likely to abort than microspores of the latter type. Exactly the opposite was found in the current study. An alternative explanation for the excess of hyperploid generative nuclei is preferential segregation after nondisjunction, the pole which gives rise to the generative nucleus might preferentially receive the extra chromosome. In summary, this study indicates that the r-xi deficiency induces nondisjunction at the first microspore division but not at the second microspore division in maize. The authors thank Funk Seeds International for providing nursery facilities in which material utilized in this study was grown, and Alan Katz for help with statistical analyses. This work was supported by Department of Energy grant 79EV and U.S. Department of Agriculture grant 6-CRCR-- to D.F.W. LITERATURE CITED HELENTJARIS, T., D. F. WEBER and S. WRIGHT, 986 Use of monosomics to map cloned DNA fragments in maize. Proc. Natl. Acad. Sci. USA 8: HELENTJARIS, T., M. SLOCUM, S. WRIGHT, A. SCHAEFER and J. NIENHUIS, 986 Construction of genetic linkage maps in maize and tomato using restriction fragment length polymorphisms. Theor. Appl. Genet. 7: KINDIGER, B., and J. B. BECKET", 985 A hematoxylin staining procedure for maize pollen grain chromosomes. Stain Technol. 6: LIN, B-Y., and E. H. COE, JR., 986 Monosomy and trisomy induced by the r-x deletion in maize, and associated effects on endosperm development. Can. J. Genet. Cytol. 8: MCCLINTOCK, B., 94 The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch. Mikrosk. Anat. : SIMCOX, K. S., J. D. SHADLEY and D. F. WEBER, 987 Detection of the time of occurrence of nondisjunction induced by the r- X deficiency in Zea mays L. Genome WEBER, D. F., 978 Nullisomic analysis of nucleolar formation in Zea mays. Can. J. Genet. Cytol WEBER, D.F., 98 Maize pollen test systems to detect nondisjunction. Environ. Health Perspect. 7: WEBER, D. F., 98 Monosomic analysis in diploid crop plants. pp In: Cytogenetics of Crop s, Edited bym. S. SWAMINATHAN, P. K. GUPTA and U. SINHA. Macmillan India Limited, New Delhi. WEBER, D. F., 986 The production and utilization of monosomic Zea mays in cytogenetic studies. pp In: Gene Structure and Function in Higher s, Edited by G. M. REDDY and E. H. COE, JR. Oxford and IBH Publishing Go., New Delhi. ZHAO,. Y., and M. G. Gu, 988 Cytogenetic Studies of Chemically-induced Parthenogenic Maize s. Acta Genet. Sin. 5: Communicating editor: B. BURR
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