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Linkage between the Centromere and a Gene Producing Nucleocytoplasmic Compatibility in Durum Wheat.

WILD RELATED SPECIES are a useful reservoir of desirable genes for widening the genetic base of wheat and to reduce the vulnerability of wheat cultivars to emerging diseases and environmental hazards. Hybrid sterility and lack of genetic recombination between wheat and alien chromosomes remain major obstacles to alien gene transfers, even though wheat cultivars can be crossed successfully with a large number of related wild species. Modern parasexual transgenic and transformation methods for directly introducing alien genes to other crop species are not routinely available for introducing alien genes into wheat cultivars. However, alien cytoplasms and chromosomes (segments) from many species, including barley (Hordeum vulgare L.) and rye (Secale cereale L.), have been introduced into wheat by cytologically monitoring the chromosomal constitution of backcross progenies from interspecific hybrids (Maan and Gordon 1988). Even when transgenic techniques improve, it will still be desirable to transfer segments of alien genomes to wheat by interspecific crosses.

In general, wheat lines carrying alien cytoplasms and alien chromosomes produce less seed and biomass than the controls in field tests (Tsuji and Maan 1981; Busch and Maan, 1978). However, wheat cultivars differ in regard to compatibility with the cytoplasms from related species. The alien cytoplasms also differ in regard to compatibility with the native nuclear genes in wheat (Maan, 1975). Cytoplasmic genes have exclusive maternal inheritance in sub-tribe Triticeae. Therefore, backcross methods can be used to substitute the nuclear genome of one species into the cytoplasm of another, provided interspecific hybrids produce functional female gametes and successive backcrosses with the paternal parent produce viable progeny (Kihara, 1951). Triticum species differ in regards to compatibility with alien cytoplasms and interspecific nucleocytoplasmic interactions produce a variety of phenotypes, including maternally inherited male sterility, delayed maturity, and reduced plant vigor in the alloplasmic wheat lines (Maan, 1975). In general, common wheat (Triticum aestivum L.; 2n = 6[chi] = 42 AABBDD) shows fewer detrimental effects as a result of cytoplasm substitution than does durum wheat (T. turgidum var. durum; 2n = 4[chi] = 28 AABB) (Sasakuma and Maan, 1978; Maan, 1978, 1983).

Triticum aestivum L. and T. timopheevii with Aegilops longissima (lo) cytoplasm have normal fertility and plant vigor. However, the nuclear genome of durum wheat in Ae. longissima cytoplasm ([lo] durum) is an incompatible combination resulting in inviable seeds (Maan, 1975). The scs (species cytoplasm specific) nuclear genes ameliorate effects of the alien cytoplasms and produce partial compatibility between the nuclear genomes of wheat and alien cytoplasms (Kihara, 1951; Maan, 1975, 1995; Tsunswaki, 1993). This is different from fertility restoration genes (Rf) which function to restore complete fertility to alloplasmic durum and wheat lines with T. timopheevii cytoplasm (Maan and Gordon, 1988). Rf genes have no effect on the incompatibility in alloplasmic (lo) durum. Most alien scs genes are located in the group 1 homoeologues (Raupp et al., 1990; Friebe et al., 1993; Suzuki et al., 1994). In this study, two scs genes were investigated. One derived from T. timopheevii is located on 1AL (long arm of chromosome 1A) of durum wheat (Maan, 1992a, b; Anderson and Maan, 1995) and another with a similar effect is located on 1DL (long-arm of chromosome 1D) from common wheat (Maan, 1994; Maan and Endo, 1991). Each scs gene produces partial compatibility between the nuclear genome of durum wheat and (lo) cytoplasm (Maan, 1992a, 1994). The (lo) scs durum lines, thus produced, are male sterile, and when crossed with the control durum, produce some plump viable seeds (with scs gene) and some shriveled inviable seeds (lacking scs gene). Thus, the chromosome carrying scs is transmitted through the plump viable seeds.

Results from RFLP mapping indirectly indicate that the scs gene on 1AL is located near the centromere (Anderson and Maan, 1995). The objectives of this study were to obtain direct evidence as to the degree of linkage between the scs gene and the centromere on chromosome 1A, and the functioning of female gametes carrying both scs genes in 13" + 1'1A + 1'1D double-monosomic plants.

MATERIALS AND METHODS

Genetic Structure and Breeding Behavior of the Durum Lines

The (lo) scs durum selection 56-1 (genotype [1A.sup.SCS]/1A) carrying a scs gene from T. timopheevii is male sterile. It has normal meiosis and produces a 1:1 ratio of female gametes with or without scs, and when crossed to the control or other durum lines produces plump and viable seed carrying scs, while those without scs are shriveled and inviable. Therefore, scs remains fixed in the male-sterile progeny from successive crosses with the control durum. Breeding behavior of scs genes in plants with normal durum cytoplasm is unknown, for there is no apparent effect on seed viability. The parental durum 56-1 (genotype 1A/1A) is the maintainer of the (1o) scs male-sterile line and was used as a control durum line in this study.

A Langdon durum disomic substitution line, where a 1D chromosome pair (genotype [1D.sup.SCS]/[1D.sup.SCS]) of common wheat substitutes for the 1A chromosome pair [LDN-CS DS 1D(1A); 13" + 1" 1D(1A)] (Joppa, and Williams, 1988), was used as a source of a scs gene on chromosome 1D. The LDN-CS DS 1D(1A) durum line is fertile and when crossed to durum produces progeny monosomic for chromosome 1A and 1D (i.e., double monosomic, dM) having the meiotic configuration of 13" + 1'1A + 1'[1D.sup.SCS] (13 pairs of durum chromosomes and one copy each of 1A and [1D.sup.SCS]). At metaphase I of meiosis, the 1A and [1D.sup.SCS] chromosomes remain unpaired and are randomly transmitted through the female gametes. The 13-chromosome female gametes seldom function and functional female gametes carry 1A, or [1D.sup.SCS], or both chromosomes in addition to the other 13 chromosomes.

A LDN dDt 1A (13" + t"1AS + t'1AL) is a double-ditelosomic 1A line of Langdon durum (Joppa, 1988). In this line (genotype 1AL/1AL, no scs gene on the long arm of chromosome 1A), the 1A chromosome pair is represented by its two telocentric arms. The LDN dDt 1A plants have 30 chromosomes, which usually form 15 pairs at metaphase I and disjoin normally during meiosis. Hybrids from a cross between dDt 1A and control durum normally have 13'+ t1t"(13" + 1'1A + t'1AS + t'1AL) at metaphase I of meiosis. In some pollen mother cells (PMCs), one telosome (t'), usually t1AS, may remain unpaired and pairing configurations in such PMCs are designated as 13" + t1" + t'. Together, the two telosomes genetically represent a complete chromosome, even though each telosome has a functional centromere, and behaves like a normal chromosome during meiosis.

Experimental Procedures

The (lo) scs durum line was crossed to LDN-CS DS 1D(1A). The resulting [1A.sup.SCS] + [1D.sup.SCS] or 1A + [1D.sup.SCS] dM [F.sub.1]S (2n = 28; 13"+2') were crossed to durum 56-1 and to LDN dDt 1A. Plants from the latter cross were cytologically identified and backcrossed to LDN dDt 1A and control durum 56-1. The plants were grown in the greenhouse.

The (lo) scs durum plants are male sterile. To produce hybrid seed, the spike to be crossed was enclosed in a glassine bag prior to anthesis, pollinated with fresh pollen from the desired male parent, and again enclosed in a glassine bag to prevent contamination by stray pollen from other wheat plants in the greenhouse. At maturity, crossed spikes were examined for the numbers of plump and shriveled seeds. Only the plump seeds known to carry a scs gene were planted, because seeds without scs were shriveled and inviable (Maan, 1992a). Sporocyte samples from each plant were taken at the appropriate stage of meiosis for cytological examination and fixed in Carnoys's solution (6 ethanol:3 chloroform:1 acetic acid). To determine chromosomal constitution of the individual plants, PMCs were smeared in a drop of acetocarmine solution on a glass slide to stain the chromosomes. The number and pairing of chromosomes at metaphase I of meiosis were examined under a light microscope.

RESULTS AND DISCUSSION

A cross between (lo) scs durum ([1A.sup.SCS]1A) and the 1D(1A) disomic substitution line of LDN durum ([1D.sup.SCS]/ [1D.sup.SCS]) produced all plump viable seeds, because they all had at least one paternal scs gene (Fig. 1). Two types of 13" + 1'1A + 1'1D dM [F1] progeny resulted ([1A.sup.SCS] + [1D.sup.SCS] or 1A + [1D.sup.SCS]) which were distinguished by their breeding behavior in regard to numbers and cytological configurations at metaphase I in the PMCs (Fig. 1).

[Figure 1 ILLUSTRATION OMITTED]

The (lo) durum (13" + 1A[scs] + 1D[SCS]) plants were crossed with control durum. Crosses produced 319 plump seeds and 34 (9 %) shriveled seeds (Fig. 1, Table 1). The shriveled seeds must have resulted from fertilization of 12-chromosome female gametes that were nullisomic for both 1A and 1D. Plump seeds from this cross produced plants with a 1A chromosome as often as ones with a 1D chromosome. Therefore, both 1A and 1D chromosomes in this cross must have a scs gene in the functional female gametes.

[TABULAR DATA 1 NOT REPRODUCIBLE IN ASCII]

A cross between 13" + 1'[1A.sup.SCS] + 1'[1D.sup.SCS] plants and a LDN dDt 1A line, however, produced 36 plump and 32 (47%) shriveled seeds (Fig. 1, Table 2). Most plants received a maternal [1A.sup.SCS] chromosome through the female gametes and those that received a maternal [1D.sup.SCS] chromosome were rare or the zygotes died (Fig. 1, Table 2). Based on the results from the control cross, plants with 13" + t1t"'[.sup.SCS] (13" + 1'[1A.sup.SCS] + t'1AS + t'1AL) and plants with 13" + [1.sup.SCS] t' + t' (13" + 1'[1D.sup.SCS] + t'1AS + t'1AL) should have occurred with equal frequency. This discrepancy is unexplained, especially in view of the results from progenies of 1A + [1D.sup.SCS] crosses.

[TABULAR DATA 2 NOT REPRODUCIBLE IN ASCII]

Plants without scs on chromosome 1A (13" + 1'1A + 1'[1D.sup.SCS]) when crossed with control durum produced more than thrice as many plump seeds as shriveled seeds (Table 1). None of the plants grown from plump seeds had 14 pairs of chromosomes, indicating that the maternal plants lacked a scs gene on chromosome 1A and only those that received a 1D chromosome were viable (Fig. 1, Table 1). When 13" + 1'1A + 1'[1D.sup.SCS] plants were crossed with LDN dDt 1A, all viable progeny received a maternal 1D chromosome (Fig. 1, Table 2). The low number of shriveled seeds in these crosses may indicate that many of the zygotes aborted at an early stage of embryogenesis-endosperm development.

A number of plants with 13" + t1t" having scs on the normal 1A chromosome were crossed with control durum (Fig. 1, Table 1). Crossed spikes had nearly equal numbers of plump seeds and shriveled seeds. If there had been a crossover between the centromere of a telosomic chromosome 1AL and scs on the long-arm of normal chromosome 1A, then some plants produced from the plump seeds should have had 13" + t1t" but all plants had 14". Therefore, no crossovers between the centromere and scs were obtained (Fig. 1, Table 1). Similarly, backcross of plants with 113" + t1t"' to LDN dDt 1A could have produced crossover progeny having a dDt 1A (2n = 30; 13" + 2t") with scs on 1AL. All viable progeny had 13" + t1t"' and no progeny with a crossover between the centromere and the scs gene were recovered (Fig. 1, Table 2). In a related study (Maan, unpublished), (1o) scs durum was crossed with dDt 1A and [F.sub.1s] (13" + t1t"', 13" + 1'[1A.sup.SCS] + t'1AS + t'1AL) were crossed to control durum resulting in 97% plants having 14" and 3% with 13" + 1'[1A.sup.SCS] + t'1AL meiotic configuration. These data supplement the results from present study indicating a close association of scs and centromere on chromosome 1A (no recombinant recovered in 188 progeny analyzed).

Plants having 13" + 1'[1D.sup.SCS] + t'1AS + t'1AL were crossed with control durum (Fig. 1). The cross produced 84% plump seeds, and 60% of these produced plants with 13" + 2' retaining [1D.sup.SCS] and 1A chromosomes. Those with one or more telosomes also had a 1D chromosome and thus, scs was not present on a telosome 1AL. Crosses of 13" + 1'[1D.sup.SCS] + t'1AS + t'1AL to LDN dDt 1A also produced more than 80% plump seeds. There was considerable variation in the chromosome configurations in the progeny of this cross (Fig. 1, Table 2). Several plants had a heteromorphic bivalent involving telosome 1AL and the 1D chromosome. In nine plants, all PMCs had 13" + 1" t1AL T1A.1D + t'1AS'. These plants had a 1A.1D translocation chromosome that paired with the long-arm of chromosome 1A (t1AL). It is clear that the female gametes and zygotes with the 1AL.1DL translocation chromosome had a selective advantage, because only 1DL had an scs gene (Maan, 1983; Maan and Endo, 1991).

A cross of the 29-chromosome (2n = 14" + 1') plants having a scs gene only in the unpaire, d 1D chromosome to control durum produced five plump seeds and 65 shriveled seeds (Fig. 1, Table 1). All three cytologically examined plants had the maternal chromosomal constitution, indicating that only the 15-chromosome female gametes having a scs gene on 1D chromosome produced viable seeds, while a majority of the 14-chromosome female gametes without scs produced shriveled seeds. The results from progenies of crosses with 13" + t1t"' + 1'[1D.sup.SCS] confirmed this deduction (Fig. 1, Table 1 and 2).

Crosses between plants with the 1A.1D translocation chromosome and control durum produced progeny with 13" + 1" 1A T1A.1D (13 pairs + 1 heteromorphic open bivalent pair between 1AL.1DL anti 1A, Fig. 1). Similarly, a cross between plants with 13" + 1" t1AL T1A.1D + t"1AS and LDN dDt 1A produced progeny with the maternal chromosome constitution, indicating that only the translocation chromosome was transmitted through the female gametes (Fig. 1). In these progeny, only the 1DL had a scs gene, 1DL remained unpaired in the open heteromorphic pair, and pairing occurred between 1AL in the translocation chromosome and the paternal telocentric 1AL, neither of which had a scs gene. The plants with 13" + 1" t1AL T1A.1D + t'1AS were maintained by using dDt 1A as a recurrent male parent. The presence of an unpaired telocentric 1AS and an open heteromorphic pair in successive crosses to dDt 1A shows that a maternal 1AL.1DL translocation chromosome and a paternal 1AL formed an open heteromorphic pair, and scs in 1DL restored seed viability. The 1AL.1DL translocation was observed in progenies from crosses between 13" + 1'1A + 1'[1D.sup.SCS] plants, or 13" + t1t"' + 1'[1D.sup.SCS], or 13" + t'1AS + t'1AL+ 1'[1D.sup.SCS] with dDt 1A. This translocation many have resulted from ectopic recombination or mis-division of chromosomes [1D.sup.SCS] and 1A, or t1AL in certain cases, in meiosis of maternal plants.

Results of the present study provide direct support for the conclusion based on RFLP results of Anderson and Maan (1995) that the scs gene is closely linked with the centromere on chromosome 1A; and consequently, we were not able to recover a plant having scs on a telosome 1AL. When given the choice, the functional female gametes carried one or both copies of scs genes on the 1A and 1D homoeologues. Additionally, translocation chromosomes were recovered because of the availability of a strong selection for the scs gene on 1DL.

ACKNOWLEDGMENTS

The authors gratefully acknowledge superb technical assistance of Kay Carlson and Joan Gordon. Also, critical reviews of the manuscript by several colleagues are greatly appreciated by the authors.

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S. S. Maan, L. R. Joppa, and S. F. Kianian(*)

S.S. Maan and S.F. Kianian, Dep. of Plant Sciences, North Dakota State Univ., Fargo ND 58105; L.R. Joppa, USDA-ARS Northern Crop Science Lab., Box 5677, North Dakota State Univ., Fargo, ND 58105. Received 1 July 1998.*Corresponding author (kianian@ badlands. NoDak.edu).

Published in Crop Sci. 39:1044-1048 (1999).
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