CYTOGENETICS OF CHROMOSOME PAIRING IN WHEAT
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1 Symposium on Meiosis : X11 nternational Congress of Genetics CYTOGENETCS OF CHROMOSOME PARNG N WHEAT RALPH RLEY Plant Breeding nstitute, Cambridge, England ABSTRACT Meiotic chromosome pairing in Triticum aestivum is controlled by genetic systems promoting and reducing pairing. The pairing of homoeologous chromosomes is prevented principally by the activity of a single locus (PA) distally located on the long arm of chromo some 5B. n certain hybrids, supernumerary chromosomes (B chromosomes) from Aegilops species can compensate for the absence of chromosome 5B by preventing or reducing homoeologous pairing. Temperature-dependent variants and colchicine sensitivity have been used to show that there are at least two stages in the 61 of meiosis at which the occurrence of meiotic pairing is determined. Wheat may differ from lily in the detailed organization of meiosis. ENOTYPES have been described in many organisms that deviated from the Gnormal course of meiosis. Those affecting the association of chromosomes at first metaphase of meiosis have been described as asynaptic or desynaptic depending upon whether or not the chromosomes were considered to have paired in prophase. Although information from pairing variants has helped in providing some understanding of the genetic control of the pairing and recombinational processes, it has not been especially useful in explaining the nature and size of the genetic systems involved nor how or when their effects are produced. However, the work that has been carried out on the genetics of chromosome pairing in wheat (Triticum aestiuum, 2n = 6x = 42) since 1957 has provided a fuller picture than is available in any other higher organism so will concentrate my attention on this. T. aestiuum is an allohexaploid species with 42 chromosomes which normally forms 21 bivalents at meiosis. t has disomic inheritance so that each chromosome pairs only with its single fully homologous partner. The cytogenetic structure of wheat was described by SEARS (1954, 1966) who showed that the 21 pairs of chromosomes can be classified into three sets each of seven pairs representing the genomes obtained from different diploid parents. The complement can also be classified into seven so called homoeologous groups each of three pairs. Homoeologous chromosomes have similar genetic activities and their relationships probably depend upon their origin from the same chromosome of the diploid progenitor of the wheat group. There is one representative of every genome in every homoeologous and of every homoeologous group in every genome (Table ). Genetics 78: September, 1974
2 ~ 194 R. RLEY TABLE 1 Classification of the chromosomes of T. aestivum Genomes Homoeologous groups A B D 1 1A 1B 1D 2 2A 2B 2D 3 3A 3B 3D 4 4A 4B 4D 5 5A 5B 5D 6 6A 6B 6D 7?A 7B 7D GENETCS OF HOMOEOLOGOUS PARNG Meiotic chromosome pairing is confined to fully homologous partner chromosomes and does not normally occur between homoeologs because of the genetic constraints that apply to all chromosomes of the complement. An activity of the long arm of chromosome 5B is principally responsible for the prevention of homoeologous pairing (RLEY and CHAPMAN 1958; SEARS and OKAMOTO 1958; RLEY 1960) though an arm of 3D has a similar but less marked effect (MELLO- SAMPAYO 1968, 1971a). RLEY and KEMPANNA (1963) showed that the interchanges that arose as a result of non-homologous recombination in the absence of chromosome 5B were between homoeologues-so providing proof of the hypothesis that the chromosomes that paired non-homologously were homoeologous. Counteracting the effects of 5BL and 3D are others as a result of which there is a general promotion of pairing. Prominent among the chromosomes with these effects are 5BS (RLEY and CHAPMAN 1967), 3B (SEARS 1954), and 5A and 5B ( FELDMAN 1966). All the initial work on the 5B pairing system relied on the use of aneuploids rom which either the entire chromosome or the long arm was deficient. To refine the genetic analysis it was necessary to induce allelic variation. Early attempts had shown that mutation could be induced in the system at high frequency (OKAMOTO 1962, 1966; RLEY, CHAPMAN and BELFELD 1966). Subsequently WALL, RLEY and CHAPMAN (1971) isolated mutants following EMS treatment. Only one of these, Mutant 10/13, has been analyzed thoroughly. The effect of the mutant is to cause homoeologous wheat chromosomes to pair in hybrids between wheat and rye although they do not normally do so and although homoeologs do not pair in wheat lines homozygous for the mutant condition. The phenotype is therefore different from that of lines entirely deficient for 5BL. When made heterozygous, the 10/13 Mutant segregates as though mutant at a single locus, and monosomic and trisomic segregation analyses show the locus to be on chromosome 5BL (WALL, RLEY and GALE 1971). Thus, apparently, homoeologous pairing in wheat is prevented by the activity of a single locus which we call Ph (for Pairing homoeologous). Telocentric linkage tests following both disomic and trisomic segregation have shown that Ph segregates independently of the centromere (Table 2). Chiasma frequency in the long arm of chromosome
3 ~ ~~~~ ~~ CHROMOSOME PARNG N WHEAT 195 TABLE 2 Segregation from the cross (T. aestivum mutant 10/13 5BL ditelo. x euploid) X S. cereale -~ 5B state Complete Telocentric Total Segregation No homoel. : homoeol. pairing Complete 5B : telocentric 5BL Linkage Total Pairing NO Homoeologous homoeologous Total a4 154 Expected xz D.F. P 1:l :l :l:l: (After WALL, RLEY and GALE 1971). 5B indicates that its length is greater than 90 map units-so it is not especially surprising that genetic linkage is not detected. Precise mapping will depend on the availability of intermediate markers. Despite the absence of phenotypic effect in plants homozygous for the mutant condition, trisomic segregation, giving wheat-rye hybrids disomic for 5B, showed the mutant to be recessive to the norcondition at the Ph locus. The diploid-like meiotic behaviour of T. aestiuum apparently depends upon the activity of the single Ph locus and is presumably therefore mediated by a single protein. The means, in terms of cellular mechanisms, by which pairing is confined to fully homologous partners is still subject to speculation but two hypotheses have been proposed. RLEY (1968) suggested that different pattern of pairing in contrasted SB genotypes might be due to differences in the time available for synapsis. n plants lacking 5BL in which homoeologs as well as homologs synapse it was postulated that the duration of zygotene is long. By contrast at the other extreme with six doses of 5BL as described by FELDMAN ( 1966) there is a reduced level of pairingeven of homologs-and this could be postulated as resulting from a short duration of zygotene, during which even the pairing of homologs is not completed. The duration of meiosis from the beginning of lepotene to the end of second telophase has been determined in a number of wheat genotypes and interspecific hybrids with and without homoeologous chromosome pairing using the sampling method described by BENNETT, CHAPMAN and RLEY (1971). Although the absence of the short arm of 5B from wheat increases the duration of meiosis by about fifteen percent there are no differences in otherwise similar genotypes with or without homoeologous pairing BENNETT. DOVER and RLEY (unpublished) nor were there any marked differences in the duration of the stages preceding pachytene. From this it can be concluded that the occurrence of homoeologous pairing is not due to a greater length of the time available for synapsis at zygotene relative to the time available in genotypes with strictly homologous pairing. However, as will be pointed out later, it may be that the
4 196 R. RLEY duration of pre-meiotic processes that affect pairing should be compared in appropriately contrasted genotypes. An alternative hypothesis has been postulated by FELDMAN (1966, 1968) to account for the occurrence of homoeologous as well as homologous pairing in some genotypes, solely homologus pairing in others and, at the most extreme, even a reduction in homologous pairing. This hypothesis suggests that the differences in pairing patterns may arise from different spatial distributions of potential pairing partners at the time that pairing is initiated. n the absence of 5BL homoeologs as well as homologs may be adjacent and co-orientated. When 5BL is disomic only homologs are adjacent and co-orientated, while when B5L is in high dose even the proximity of homologs is diminished. Subsequently FELDMAN, MELLO- SAMPAYO and SEARS (1966) and FELDMAN, MELLO-SAMPAYO and AVV (1972) provided evidence for an extension of the idea, asserting that a similar range of spatial relationships also occurs in somatic cells. There is as yet no confirmation of the hypothesis that genetically determined differences in the occurrence of homoeologous pairing are or are not mediated by changes in the spatial ordering of chromosomes. However, the notion has considerable appeal, not least because the precise positioning of chromosomes within the nucleus, possibly by means of specific membrane attachment points, would explain the general absence of bivalent interlocking in all higher organisms. At present there seems little probability that a verifiable explanation of the genetic control of homoeologous pairing will be derived from a hypothesis based on chromosome mechanics. t would be more profitable to attempt to exploit the available genetic variation to search for biochemical distinction and so provide a point of experimental access. PREVENTON OF HOMOEOLOGOUS PARNG BY SUPERNUMERARY CHROMOSOMES Considerable attention has been given to the possible evolutionary origin of the system determining the diploid-like meiotic behaviour of polyploid wheat (RLEY and LAW 1965). No diploid relative has been found with a genetic activity corresponding to that of the Ph locus of T. aestiuum. Usually one or other of two patterns of meiotic pairing takes place in hybrids between T. aestiuum and related diploid species. Either there is no homoeologous pairing so long as 5B is presentthat is the Ph locus continues to be effective-but homoeologous pairing occurs when 5B is absent. Alternatively there is homoeologous pairing even in the presence of 5B-that is, the genome of the diploid introduces genes dominant or epistatic to Ph (RLEY and CHAPMAN 1966). More recently it has been found that within several species genetic variation may be present and that in hybrids with wheat either the Ph activity is fully effective, and there is little homoeologous pairings, or there may be varying amounts of homoeologous pairing MELLO- SAMPAYO 1971b; KMBER and ATHWAL 1972; DOVER and RLEY 1972a). However, even in these instances, where there is intra-specific variation in the capacity to promote homoeologous pairing, no evidence has yet been provided of an activity like that of Ph (DOVER and RLEY ).
5 CHROMOSOME PARNG N WHEAT 197 TABLE 3 Mean chromosome pairing in F, hybrids from the cross Ae. speltoides x T. boeticum with and without a supernumerary chromosome derived from Ae. speltoides (30 cell/plant) Range of plant means Chromosome No. Triv. and Supernumerary no. hybrids Univ. Biv. quad. Chiasmata None & M One t has been shown, however, that in T. aestivum x Aegilops mutica hybrids there is compensation for the absence of chromosome 5B, indicated by the inhibition of homoeologous pairing, if supernumerary (or B) chromosomes are present (DOVER and RLEY 1972b). n the wheat group, therefore, as in Lolium (EVANS and MACEFELD 1973) supernumeraries can prevent, or reduce, homoeologous pairing. The parallel between the original report of EVANS and MACE- FELD (1973) for Lolium and that of RLEY, CHAPMAN and MLLER (1973) for the wheat group is exact at the diploid level. The 14-chromosome hybrid Aegilops speltoides X Triticum boeticum has high pairing in the absence of supernumeraries but low pairing in their presence (Table 3), just like the hybrids of Lolium temulentum X Lolium perenne. EVANS and MACEFELD report that homoeologous chromosomes pair in the presence of supernumeraries but that chiasma formation does not follow. This may imply that the effect of the supernumeraries is not on the processes that in wheat are affected by the Ph system. On the other hand, if the supernumeraries do affect meiotic chromosome pairing through the same causal processes as Ph, then they must obviously be regarded as another possible source of origin of the diploidizing system of wheat. CHROMOSOME PARNG DETERMNED AT G mportant evidence on the meiotic processes in wheat has been obtained from work on a temperature-dependent pairing pattern that occurs in the deficiency of chromosome 5D (RLEY 1966, BAYLSS and RLEY 1972a). n most T. aestivum genotypes this genetic activity is duplicated, but in the variety Chinese Spring chromosome 5D alone stabilize meiotic chromosome pairing against pairing failure induced by extremes of temperature. Expressing the level of synapsis in terms of chiasma frequency (Figure 1 ) synapsis in plants lacking 5D resembles that in euploids between 19" and 29". Above and below these temperatures chiasma frequency is sharply reduced in 5D-deficient plants but little changed in euploid (BAYLSS and RLEY 1972a). Clearly with a sharp response to temperature like this it was possible to determine the stage of the meiotic process which must be exposed to extremes of temperature for pairing to fail. BAYLSS and RLEY (1972b) carried out temperature-switch experiments from 15" to 20" and the reciprocal and determined the time that elapsed before chiasma frequency settled to the level appropriate for the final temperature. n the case of the transfer from 15" to 20" there was a period
6 198 1 R. RLEY A 1.0 U! E CJ r r U n v) - 6 E 04- N5D.T5B D--a EUPLOD t TEMPERATURE "C FGURE 1.-The response of meiotic chromosome pairing, scored as chiasmata per chromo. some, to temperature, in the T. aestiuum genotypes euploid, nullisomic 5D tetrasomic 5B, N5D T5B) and nullisomic 5D. (BAYLESS and RLEY 1972a) of 6.5 hours over which chiasma frequency changed to that appropriate to 20" from that appropriate to 15". The midpoint of this change was 38.7 hours from the time of the switch from 15" to 20" (Figure 2). Using the methods of BENNETT, CHAPMAN and RLEY (1971) the duration of meiosis at 20" was determined to be 23.5 hours in normal wheat and 25.0 hours in the line lacking 5D used in the temperature-switch experiments. n this sense, meiosis is considered to last from the initiation of leptotene to second telophase and the differences between the genotypes were probably not significant in relation to the errors in the methods. However, the extent of pairing was measured by chiasma frequency at first metaphase which occurred about 16 hours after the commencement of meiosis. On this basis the temperature-sensitive stage was 38.7 hours before first metaphase or 22.7 hours before the initiation of meiosis at leptotene. Since BENNETT and SMTH (1972) have shown that the immediately premeiotic DNA synthesis lasts for about 10 to 12 hours and takes place immediately prior to leptotene, the temperature-sensitive stage not only precedes the occurrence of the visible nuclear changes called "meiosis" but also the meiotic S phase. From this we learn that events occur in the G1 of meiosis that are crucial from chromosome pairing (Figure 3).
7 ~ CHROMOSOME PARNG N WHEAT 199 H NSDT5B 3-4 EUPLOD,,,,,, ; TME N HOURS FROM TEMPERATURE CHANGE ' TME N HOURS FROM TEMPERATURE CHANGE FGURE 2.-Response of meiotic chromosome pairing to the change of temperature from 15 C to 20 C in euploid plants of T. aestiuum and in genotypes nullisomic 5D and tetrasomic 5B (N5D T5B). The results shown in the graph on the left were derived from sampling at intervals of 24 hours after the temperature change and those in the graph on the right from sampling at intervals of 3 hours after the rhanep (RAW FSS and Rrr rv 1972h) METAPHASE ZYGOTENE - n a L - 20.E 30 Y 5-40 TEMPERATURE SENSTVE STAGE PREMEOTC... U TCC+._"." FGURE 3.-Relationships in the timing of development of the stage that in 5D deficiency is sensitive to low temperatures in meiotic chromosome pairing in comparison with other components of the meiotic cell cycle.
8 200 R. RLEY Evidence indicating the importance of pre-meiotic events on meiotic chromosome pairing was derived from examinations of the effects of colchicine (DRS- COLL, DARVEY and BARBER 1967; and DOVER and RLEY 1973). Exposure of the cells of T. aestivum immediately after the final pre-meiotic mitosis to 0.5 per cent colchicine caused asynapsis, but application of colchicine later than this had no effect on the pattern of meiotic chromosome pairing. n 5D-deficient wheat it appears that the pre-meiotic stage which is sensitive to colchicine may precede that sensitive to temperature by 10 to 15 hours at 20". This suggests that the build up to meiotic chromosome pairings is prolonged and multi-staged and directs attention to some of the studies of premeiotic development carried out by BEN- NETT and his colleagues (BENNETT et al., 1973). This work shows that the cell cycle time extends in archesporial cells as meiosis approaches. The immediately pre-meiotic cycle lasts about 55 hours, the penultimate cycle 35 hours and the one before that 25 hours. There is a long hold of between 48 and 103 hours at the 2C DNA content during which the previously asynchronous cells of the archesporial tissue are assembled in the meiotic G1. t appears that the release from this G hold may be into the S phase, but this is uncertain. n wheat therefore, there is a prolonged meiotic G during which processes are initiated that finally result in meiotic chromosome pairing. n part, the preparation for chromosome pairing may involve the production of appropriate spatial ordering of potential pairing partners. This conclusion is prompted not only by asynapsis that occurs following exposure to colchicine soon after the immediately premeiotic mitosis but also by the pattern of pairing that occurs when the spindle formation is inhibited at the final mitosis. When this occurs the chromosome number of the pollen mother cell is doubled but, despite the tetrasomic status of each chromosome, only bivalents are formed. t is presumed that the bivalents are formed between chromosomes that were formerly sister chromatids and that, in the absence of anaphase and other movements, chromosomes derived from non-sister chromatids are not brought into positions that permit quadrivalent formation. So events immediately following the premeiotic mitosis influence pairing probably through their effects on the co-orientation and juxtaposition of potential partners. Not only is the temperature-sensitive stage separate from these occurences in time, but there is direct evidence of a functional difference. DRSCOLL and DARVEY (1970) showed that when a genotype of wheat was given a colchicine exposure that caused general asynapsis there was still chiasma formation, and therefore pairing, between two arms of an isochromosome. By contrast, in a wheat genotype deficient for chromosome 5D and exposure to 15" there was no chiasma formation, and therefore inadequate pairing, between the arms of an isochromosome (RLEY and BAYLSS 1972a and b). Thus when proximity is retained, despite the colchicine effect, pairing still occurs but enforced proximity is not sufficient to overcome the temperature effect. This suggests that the system has advanced to a lower order in the address system by the temperature-sensitive stage.
9 CHROMOSOME PARNG N WHEAT 20 1 A question is immediately posed concerning the relationships of the effects of meiotic pairing of the long arm of chromosome 5B and 5D. On the evidence of the behavior of isochromosomes, 5D apparently affects a process in meiotic G1 that is independent of the relative positions of the potential partners. One hypothesis asserts that the action of 5B is mediated through its effects on the relative position of potential partners. f the activities of 5B and 5D are determined by homoealleles, the time and mode of action of the 5D system suggests that the spatial hypothesis cannot be applied to the 5B effect. Alternatively the observations available may be taken to imply that the loci involved are not homoeologous. The determination in wheat of meiotic chromosome pairing by processes occurring in G raises questions about the way that this relates to the well described control of pairing in lily (HOTTA, TO and STERN 1966; HOTTA and STERN 1971). n lily there is semi-conservative replication and synthesis of a distinctive fraction of DNA at zygotene in the absence of which pairing does not occur. As has been shown by RLEY and BENNETT (1971) and by FLAVELL and WALKER (1973) DNA synthesis occurs throughout meiosis in wheat. However, the synthesis at zygotene is not distinctive in base ratio nor does inhibition of synthesis prevent chromosome pairing. Apparently the systems of pairing regulation are different in wheat and lily, so even within the same plant family the details may differ in the processes underlying meiosis. n the former there is more than one significant premeiotic process. This of course implies differences in the genetic control of meiosis between wheat and lily which it is perhaps not surprising to find in groups that have diverged widely in evolution, especially in view of the range of genetic diversity that can be found or created within the wheat group. Apart from their intrinsic interest, and their value in practical plant breeding, genetic differences either like those within wheat or between wheat and lily provide the points of entry for detailed causal analyses. The next stages in the investigation of meiosis will rely heavily upon the exploitation of genetic variation in such casual analyses. The general lesson to be learned from the present work is that the meiotic process commences before the morphologically distinctive stages occur. LTERATURE CTED BAYLSS, M. W. and R. RLEY, 1972a An analysis of temperature-dependent asynapsis in Triiicum aestiuum. Genet. Res. 20: , 1972b Evidence of premeiotic control of chromosome pairing in Triticum aestiuum. Genet. Res. 20: BENNETT, M. D., V. CHAPMAN and R. RLEY, 1971 The duration of meiosis in pollen mother cells of wheat, rye and Triticale. Proc. Rog. Soc. B. 178: BENNETT, M. D., M. K. RAO, J. B. SMTH and M. W. BAYLSS, 1973 Cell development in the anther, the ovule, and the young seed of Triticum aestiuum, L. var. Chinese Spring. Phil. Trans. Roy. Soc. B. 266: BENNETT, M. D. and J. B. SMTH, 1972 The effect of polyploidy on meiotic duration and pollen development in cereal anthers. PTOC. Roy. Soc. B. 181: DOVER, G. A. and R. RLEY, 1972a Variation at two loci affecting homoeologous meiotic chromosome pairings in Triticum aestiuum x Aegilops mutica hybrids. Nature New Biology 235: , 1972b Prevention of pairing of hommlogms meiotic chromosomes of wheat by an activity of supernumerary chromosomes of Aegilops. Nature 240:
10 202 R. RLEY --, 1973 The effect of spindle inhibitors applied before meiosis on meiotic chromosome pairing. J. Cell Sci. 12: DRSCOLL, C. J., N. L. DARVEY and H. N. BARBER, 1967 ploid wheat. Nature 216: Effect of colchicine on meiosis of hexa- DRSCOLL, C. J. and N. L. DARVEY, 1970 Chromosome pairing: effect of colchicine on an isochromosome. Science 169: EVANS, G. M. and A. J. MACEFELD, 1973 The effect of B chromosomes on homoeologous pairing in species hybrids.. Lolium temulentum x Lolium perenne. Chromosoma 41 : FELDMAN, M., 1966 The effect of chromosomes 5B, 5D and 5A on chromosomal pairing in Triticum aestiuum. Proc. Natl. Acad. Sci. US. 55: , 1968 Regulation of somatic association and meiotic pairing in common wheat. Proc. 3d nt. Wheat Genet. Symp FELDMAN, M., T. MELLO-SAMPAYO and L. AVV, 1972 Somatic association of homoeologous chromosomes in Triticum Qestiuum. Chromosoma 37 : FLAVELL, R. B. and G. W. R. WALKER, 1973 The occurrence and role of DNA synthesis during meiosis in wheat and rye. Expl. Cell Res. 77: HOXTA, Y., M. m and H. STERN, 1966 Synthesis of DNA during meiosis. Proc. Natl. Acad. Sei., U.S. 66: HOTTA, R. and H. STERN, 1971 Analysis of DNA synthesis is during meiotic prophase in Lilium. J. Mol. Biol. 55: KMBER, G. and R. S. ATHWAL, 1972 Reassessment of the course of evolution of wheat. Proc. Natl. Acad. Sci. US. 69: No. 4, MELLO-SAMPAYO, T., 1968 Homowlogous chromosome pairing in pentaploid hybrids of wheat. Proc. 3d nt. Wheat Genet. Symp , 1971a Genetic regulation of meiotic chromosome pairings by chromosome 3D of Triticum aestiuum. Nature New Biol. 230: 22- W. -, 1971b Promotion of homoeologous pairing in hybrids of Tn;icum aestiuum X Aegilops longissima. Genet. berica 23: 1-9. OKAMOTO, M., 1962 Mutation of a gene (or genes) for asynapsis and its use in plant breeding. Rept. Kihara nst. Biol. Res. 13: , 1966 Studies on chromosome 5B effects in wheat. Prac. 2nd nt. Wheat Genet. Hymp. Hereditas (Suppl.)%: RLEY, R., 1960 The diploidisation of polyploid wheat. Heredity 15: , 1966 Genotype-environmental interactions affecting chiasma frequency in Triticum aestiuum. n: Chromosomes Today. Vol. 1. Edited by C. D. DARLNGTON and K. R. LEWS. Oliver and Boyd, Edinburgh and London.-, 1968 The basic and applied genetics of chromosome pairing. Proc. 3rd nt. Wheat Genet. Symp RLEY, R. and V. CHAPMAN, 1958 Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182: , 1966 Estimates of the homoeology of wheat chromosomes by measurements of differential affinity at meiosis. pp n: Chromosome Manipulations and Plant Genetics. Edited by R. RLEY and K. R. LEWS. Oliver and Boyd, Edinburgh and London. -, 1967 Effects of 5BS in suppressing the e x p " of altered dosage of 5BL on meiotic chromomme pairing in Triticum aestivum. Nature 216: RLEY, R., V. CHAPMAN and A. M. BELFELD, 1966 nduced mutation affecting the control of meiotic chromosome pairing in Triticum aestiuum. Nature 211 : RLEY, R., V. CHAPMAN and T. E. MLLER, 1973 The determination of meiotic chromosome pairing. Proc. 4th nt. Wheat Genet. Symp. pp RLEY, R. and C. KEMPANNA, 1963 The homoeologous nature of the non-homologous meiotic pairing in Triticum aestiuum deficient for chromosome V(5B). Heredity 18:
11 CHROMOSOME PARNG L WHEAT 203 RLEY, R. and C. N. LAW, 1965 Genetic variation in chromosome pairing. Advan. Genet. 13: SEARS, E. R., 1954 The aneuploids of common wheat. Res. Bull. mo. a&. Exp. Stn , 1966 Nulisomic-tetrasomic combinations in hexaploid wheat. n: Chromosome Manipulations and Phnt Genetics. Edited by R. RLEY and K. R. LEWS. Heredity (SuDpl.) 20: SEARS, E. R. and M. OKAMOTO, 1948 ntergenomic relationships in hexaploid wheat. Proc. Xth ntern. Congr. Genet. 2: WALL, A. M., R. RLEY and V. CHAPMAN, 1971 Wheat mutants permitting homoeologous meiotic chromosome pairing. Genet. Res WALL, A. M., R. RLEY and M. D. GALE, 1971 The position of a locus on chromosome 5B of Triticum aestivum affecting homoeologous meiotic pairing. Genet. Res. 18:
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