timopheevii to durum and bread wheat and the location of
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1 The transfer of leaf rust resistance from Triticum timopheevii to durum and bread wheat and the location of one gene on chromosome 1A Dapeng Bai 1, D.R. Knott 2, and Janice Zale 3 1 USDA, ARS, SP Range Research Station, th Street, Woodward, Oklahoma, 73801, USA; 2 Department of Crop Science and Plant Ecology, University of Saskatchewan, 51 Campus Drive, Saskatoon, Saskatchewan, Canada S7N 5A8; Braemar Drive, Kamloops, British Columbia, Canada V1S 1H4. Received 13 November 1997, accepted 17 May Bai, Dapeng, Knott, D. R. and Zale, Janice The transfer of leaf rust resistance from Triticum timopheevii to durum and bread wheat and the location of one gene on chromosome 1A. Can. J. Plant Sci. 78: Triticum timopheevii (Zhuk.) Zhuk. is noted for its resistance to diseases including leaf and stem rust of wheat. Only one gene (Lr18) for leaf rust resistance has been transferred from T. timopheevii to bread wheat. The objectives of this work were to study the inheritance of leaf rust resistance in five accessions of T. timopheevii and to transfer genes for resistance into durum and bread wheats. A diallel set of crosses was made among five T. timopheevii accessions that gave a fleck infection type with an isolate of leaf rust race CBB. None of the populations of the 10 crosses segregated for resistance, indicating that the five accessions all had at least one gene for resistance in common. Several accessions were crossed and backcrossed twice to durum and to bread wheat. At least three genes for leaf rust resistance were transferred to durum wheat and one to bread wheat. The gene transferred to bread wheat and one of those transferred to durum wheat conditioned good resistance to a set of 10 diverse races of leaf rust. Resistance conditioned by all three genes was dominant in durum wheat but the one gene was recessive in bread wheat. Monosomic analysis of the bread wheat line showed that the gene is on chromosome 1A. It should be useful in breeding for leaf rust resistance in both durum and bread wheat. Key words: Triticum timopheevii, leaf rust resistance, durum wheat, bread wheat Bai, Dapeng, Knott, D. R. et Zale, Janice Transfert de la résistance à la rouille des feuilles de Triticum timopheevii au blé dur et au blé de panification et emplacement d un gène sur le chromosome 1A. Can. J. Plant Sci. 78: Triticum timopheevii (Zhuk.) Zhuk. est connu pour sa résistance aux maladies, notamment aux rouilles des feuilles et de la tige du blé. Un gène seulement (Lr18) de la résistance à la rouille des feuille, a jusqu ici été transféré de T. timopheevii au blé de panification. L objet de nos travaux était d étudier le mode de transmission de la résistance à la rouille des feuilles chez 5 obtentions de T. timopheevii et de transférer les gènes de résistance au blé dur et au blé panifiable. Une batterie de croisements diallèles parmi les 5 obtentions de T. timopheevii a donné une réaction en moucheture en présence d un isolat de la race CBB de la rouille des feuilles. Aucune des populations des 10 croisements ne manifestait de ségrégation pour la résistance, laissant supposer que les 5 obtentions avaient au moins un gène de résistance en commun. Plusieurs obtentions étaient croisées puis rétrocroisées deux fois au blé dur et au blé de panification. Au moins 3 gènes de résistance à la rouille des feuilles ont été transférés et un au blé de panification. Le gène transféré à ce dernier et un des trois transférés au blé dur se manifestaient par une bonne résistance à un jeu de 10 races de la rouille des feuilles. La résistance modulée par les 3 gènes transférés au blé dur était de type dominant mais le gène transféré au blé panifiable était récessif. L analyse monosomique de cette dernière lignée a en outre révélé que le gène est situé sur le chromosome 1A. Il devrait avoir une utilité dans la sélection pour la résistance à la rouille des feuilles chez les deux types de blé. Mots clés: Triticum timopheevii, résistance à la rouille des feuilles, blé dur, blé tendre (panifiable) Triticum timopheevii (Zhuk.) Zhuk. is a good source of resistance to several diseases of wheat including leaf rust (Puccinia recondita Rob. ex Desm. f. sp. tritici) and stem rust (Puccinia graminis Pers. f. sp tritici) (McIntosh and Gyarfas 1971). The species is a tetraploid that carries the A genome in common with durum wheat (T. turgidum L., AABB) and bread wheat (T. aestivum L., AABBDD), plus a second genome, G, that is related to the B genome (Kimber and Sears 1987). It should be easier to transfer genes from the A genome to the homologous genome in durum or bread wheat, than to transfer them from the G genome to the homoeologous B genome. Pairing and crossing-over will be more restricted in the latter case. Triticum timopheevii crosses fairly readily with both durum and bread wheat, and embryo rescue is not necessary to produce hybrid plants. Four identified genes for stem rust resistance and one for leaf rust resistance have been transferred from T. timopheevii to bread wheat Sr36, Sr40, and Sr Tt3 on chromosome 2B, Sr37 on 4B and Lr18 on 5B (see McInstosh et al. [1995] for references). In addition, Allard (1949) reported the transfer to bread wheat of an unnamed gene for leaf rust resistance. Interestingly, all the 2 To whom correspondence should be addressed. 683 Abbreviations: IT, infection type; LR CBB, leaf rust ace CBB; SR TMH, stem rust race TMH
2 684 CANADIAN JOURNAL OF PLANT SCIENCE genes whose locations have been identified are on B genome chromosomes. This may just be chance or it may mean that the genes for rust resistance in T. timopheevii are concentrated in the G genome. In any case, it does indicate that it is relatively easy to transfer genes from the G genome to the B genome. McIntosh (1983) suggested that T. timopheevii carries additional genes for resistance to leaf rust. In most years, leaf rust is the most widespread of the three wheat rusts in the central plains of North America, and appears to be the most threatening. Since the genes for resistance in T. timopheevii could be of value to wheat breeders, it was decided to study the inheritance of resistance and then transfer the genes into durum and bread wheats. MATERIALS AND METHODS Nine accessions of T. timopheevii from diverse sources were tested with an isolate of leaf rust race CBB (LR CBB) (Table 1). Five, TT1, TT8, TT16, TT21 and TT33, were selected for genetic study and a diallel set of crosses was made among them. The populations were tested with LR CBB. All nine accessions were used as male parents in crosses with two durum wheats, Cappelli ph1c from Italy (the gene ph1c allows pairing between homoeologous chromosomes) or RL6089, a leaf rust susceptible durum obtained from the Agriculture and Agri-Food Canada, Cereal Research Centre, Winnipeg. Five of the accessions were also crossed as male parents with bread wheats, Thatcher (Tc), a Marquis derivative (Prelude/8*Marquis) (PM), Chinese Spring (CS) or Chinese Spring ph1b (CS-ph1b). The hybrids were backcrossed twice to durum or bread wheat, although not always to the same parent used in the cross. The hybrids, and and to F 4 generations were tested with LR CBB. Homozygous resistant backcross lines were obtained, usually in the generation. They were increased and tested, along with all of the parents, with LR CBB plus isolates of a diverse group of nine leaf rust races. With any one race, all of the lines were tested at the same time under the same conditions. All of the leaf rust isolates were obtained from the Agriculture and Agri-Food Canada, Cereal Research Centre at Winnipeg. Their original race designations were 1, 15 (now CBB), 58, 70, 70B, 75, 83, 100, 104 and 161. Four of the isolates have been lost but virulence formulas (effective/ineffective genes) for the remaining six are: Race 1-3, 3ka, 9, 10, 11, 13, 14b, 16, 17, 23, 25, 26, 28, 33 / 12, 14a, 18, 20, 30 Race 15(CBB) - 1, 2a, 2b, 2c, 3ka, 9, 11, 16, 17, 18, 21, 24, 26, 30 / 3, 10, 13, 14a, 14b, 22b, 23 Race 58-3ka, 9, 11, 13, 16, 17, 25, 26, 30 / 3, 10, 12, 14a, 14b, 18, 20, 23, 28, 33 Race 100-3ka, 9, 17, 25, 26, 30 / 3, 10, 11, 12, 13, 14a, 14b, 16, 18, 20, 23, 28, 33 Race 104-3ka, 9, 11, 16, 17, 18, 25, 26, 30, 33 / 3, 10, 12, 13, 14a, 14b, 20, 23, 28 Race 161-3ka, 9, 11, 14a, 16, 20, 23, 25, 26, 30, 33 / 3, 10, 12, 13, 14a, 17, 18, 28 Table 1. Origin of the parents and their infection types with leaf rust race CBB Species and designation Abbreviation Origin Infection type T. timopheevii PI TT1 Poland 0; PI TT7 Switzerland 0; CI TT8 U.S.A. 0; CI TT10 Greece 0; PI TT16 Australia 0; PI TT19 Hungary 0; PI TT21 U.S.S.R 0; PI TT23 Switzerland 0; PI TT33 Switzerland 0; T. turgidum RL6089 RL Cappelli-ph1c Cap-ph1c 1 + T. aestivum Thatcher Tc 4 Prelude/8* Marquis PM 4 Chinese Spring CS 4 Chinese Spring-ph1b CS-ph1b 4 However, Dr. J. Kolmer, Agriculture and Agri-Food Canada, Cereal Research Centre, Winnipeg, reports that race 70 is SBD, 70B may be the same race with virulence on LrB and race 83 is PBL. He had no information on race 75 (personal communication). A monosomic analysis was done on a homozygous resistant F 4 line derived from a backcross to Thatcher. The 14 Chinese Spring lines monosomic for the A- and B-genome chromosomes were used as female parents in crosses with the resistant line. The monosomic plants were selected and their spikes bagged to prevent outcrossing. Small populations were tested with LR CBB. Root tip chromosome counts were done on resistant seedlings. Mitotic chromosome counts were done on root tip cells and meiotic counts on spikes of hybrids and backcrosses. Root tips were collected, pretreated in a mixture of colchicine (0.05%), 8-hydroxyquinoline (0.025%) and dimethyl sulfoxide (40 drops per 100 ml) for about 4 h. They were then transferred into 2% orcein in 45% acetic acid for 4 d. Finally, they were transferred into 45% acetic acid, heated to boiling and squashed (Mujeeb-Kazi and Miranda 1985). Spikes for meiotic counts were collected, fixed in Carnoy s fixative (6 absolute ethyl alcohol: 3 chloroform: 1 acetic acid) for 48 h and stored in 70% alcohol in a refrigerator at about 4 C. Anthers were stained in alcohol-acidcarmine (Snow 1963) for 48 h and squashed in 45% acetic acid. Rust tests were carried out in a greenhouse maintained as near as possible to 20 C during the day and 15 C at night. Depending on the time of year, the temperature rose above 20 C on sunny days despite the use of coolers. Supplementary fluorescent lighting was used to maintain an 18-h daylength. Seeds were planted in 15-cm-diameter pots. Seedlings at the two-leaf stage were inoculated with leaf rust spores suspended in soltrol, a light mineral oil (Phillip s Petroleum Co., Bartlesville, OK). The inoculated plants
3 BAI ET AL. TRANSFER OF LEAF RUST RESISTANCE TO WHEAT 685 Table 2. Seed set and infection types for crosses between T. timopheevii accessions and durum or bread wheats, and seed set in backcrosses IT of Species and Number of Seed set plants to Seed set in crosses florets (%) LR CBB backcrosses (%) Durum wheat RL6089/TT /TT = 15.6 /TT = 6.3 /TT = 9.4 /TT = /TT = /TT = 7.1 /TT = 8.3 Cappelli-ph1c/TT ; /TT ; Bread wheat CS/TT CS-ph1b/TT /TT Tc/TT PM/TT /TT were then kept in a chamber with a humidifier for about 18 h. After d the infection types (ITs) were read on a 0 to 4 scale, using the system of Stakman et al. (1962). Infection types 0, 1 and 2 were considered resistant and 3 and 4 susceptible. RESULTS Parents The nine T. timopheevii accessions gave 0; ITs with LR CBB (Table 1). Diallel Crosses For the 10 crosses involving the five selected, resistant T. timopheevii accessions, 116 to 345 seedlings were tested with LR CBB. All 2163 seedlings gave 0; or 1 = ITs, essentially the same as the parents. Thus, the five accessions carry at least one gene for resistance in common. Transfer of Resistance to Durum Wheat Eight of the accessions were crossed with RL 6089 durum and two with Cappelli-phlc (Table 2). Seed set ranged from 15.0 to 50.0%. All of the hybrids had good resistance to LR CBB, showing that resistance was dominant. The hybrids with RL6089 had slightly higher ITs of 1 to 1 + than the accessions (IT 0;). The hybrids with Cappelli-ph1c, which is resistant (IT 1 + ), had the same IT (0;) as the T. timopheevii parents. All of the hybrids were self-sterile except for one plant of the cross, RL6089/TT1, which set 22 seeds. The seed set in five backcrosses to RL6089 was fairly low, ranging from 6.3 to 15.6% (Table 2). Backcrosses on the two hybrids involving Cappelli-ph1c were not successful. Three second backcrosses, RL6089/TT7//2*RL6089, RL6089/TT10//2* RL6089 and RL6089/TT33//2*RL6089, were made. The generations of each backcross segregated differently for resistance to LR CBB, 48R:27S, 81R:61S and 17R:87S, respectively. From each backcross, homozygous resistant or F 4 lines were developed and tested with 10 races of leaf rust (Table 3). From the second backcross of TT7 to RL6089, six lines homozygous for resistance to LR CBB were developed and tested. There appeared to be four types of lines showing small differences in reaction to some of the 10 races (Table 3). The lines showed intermediate levels of resistance to most races. Unfortunately, the two races, 58 and 70B, to which the lines showed the most variation in ITs, have been lost and no further testing is possible. Some of the differences in ITs may be due to differences in temperature in the greenhouse during the testing. It is possible that all six lines carry the same gene. Seven lines homozygous for resistance to LR CBB were produced from the TT10 backcross and tested. Five of the lines gave good resistance to all 10 races (Table 3) and appear to carry the gene giving high resistance in the T. timopheevii accessions. The other two lines gave similar reactions except to race 70B and may carry the same gene. Again, since 70B has been lost, the lines cannot be retested. The two lines are clearly different from the lines derived from TT7. Two lines homozygous for resistance to LR CBB were produced from the TT33 backcrosses and tested. The two lines gave similar infection types (Table 3) and probably carry the same gene. They are also fairly similar to the bottom two lines derived from TT10 (Table 3). Meiotic chromosome counts were done on 7 susceptible and 33 resistant, plants from three crosses. All susceptible plants had 14II of chromosomes. Of the resistant plants, 26 had 14II of chromosomes, but 7 from one cross had 13II + 1III (some cells 14II + 1I). Transfer of Resistance to Bread Wheat Five of the accessions were crossed with bread wheats and seed set ranged from 5.0 to 42.9% (Table 2). Embryo culture
4 686 CANADIAN JOURNAL OF PLANT SCIENCE Table 3. Infection types for durum and bread wheat lines with genes for leaf rust resistance derived from T. timopheevii, tested with isolates of 10 leaf rust races No. of Infection type with leaf rust race Backcross or parent lines 1 CBB B RL6089/TT7// *RL RL6089/TT10// 5 0;1-0;1-0;1 0;1 1 = 1 1 = 1 + 0;1 0;1-0;1 = 0;1 2*RL = RL6089/TT33// * Tc/TT21//2*Tc 3 1 = 1 = 1-0;1 = 1 = 1-1 = 1-1 = 0;1 = 0;1 = 0; RL Tc TT accessions 9 0; 0; 0; 0; 0; 0; 0; 0; 0; 0 was not required to produce hybrid plants. Most of the plants were sterile but two plants from the cross, PM/TT23, produced 64 seeds. Contrary to the results for the hybrids with the durum wheat RL6089, the plants were susceptible to LR CBB (ITs 3 and 4) (Table 2). As expected, all plants were also susceptible. Plants from three of the hybrids were successfully backcrossed to bread wheat, not always to the parent used in the cross. In some cases the appropriate pollen was not available when needed. Only three plants were obtained from the backcross CS ph1b/tt8//cs and no resistant plants were recovered after a further backcross followed by selfing. The cross Tc/TT21 was backcrossed twice to Tc. All 17 plants tested were susceptible to LR CBB. Of eight families tested, two segregated. Three resistant plants proved to have 21II of chromosomes at meiosis. Three homozygous resistant F 4 lines were produced and tested with 10 races. All three lines were nearly as resistant as the parent TT21 (Table 3). The cross, PM/TT33, was backcrossed to PM and all six plants were susceptible to LR CBB. One plant was self-fertile. Fifty-eight plants were tested with LR CBB and 10 were resistant (ITs 1, 1 + or 2). Of the 10 families, one was homozygous for resistance and five segregated, but four appeared to be homozygous susceptible. Meiotic chromosome counts on 15 plants from the homozygous resistant family showed that they all had 14II of chromosomes. Counts on 20 resistant plants from the segregating families ranged from 14II to 16II + 2I. The low chromosome numbers in this material after one backcross to bread wheat were surprising. No further backcrosses were made. Chromosome Location of One Gene for Resistance One of the Tc backcross lines having good resistance to all 10 leaf rust races was used as the pollen parent in crosses Table 4. Results of chromosome counts on seedlings in families from resistant plants from crosses between Chinese Spring monosomics 1A, 2A 6A and 7A and a homozygous leaf rust resistant line from the backcross, Tc/TT21//2*Tc Number of families Chromosome Only disomic plants Seg. monosomics 1A 6 2 2A 1 6 6A 1 3 7A 2 4 with plants monosomic for the A- and B-genome chromosomes in CS. Root-tip counts were done on five or six plants of each line and the monosomic plants were selected for crossing. Because resistance is recessive in hexaploids, it was not expected that either or analysis would identify the location of the gene, and this proved to be the case. All the plants were susceptible to LR CBB and no critical cross was evident in the (data not given). Resistant plants were saved and root tip counts done on as many as possible. In the critical monosomic cross, all of the resistant plants should have 21II of chromosomes while in the non-critical crosses about three-quarters of the plants should be monosomic. A preliminary analysis eliminated chromosomes 3A, 4A and 5A and all of the B-genome chromosomes. In each case, some of the resistant plants were monosomic or nullisomic. More extensive tests were carried out on plants of the remaining crosses involving monosomics 1A, 2A, 6A and 7A for which the data were not clear. Root tip counts were done on four seedlings from 4 to 8 resistant plants of each cross. In a few cases, counts were obtained on only three seedlings. Chromosomes 2A, 6A and 7A were eliminated as the critical chromosome because the majority of the families segregated monosomic plants, showing that the resistant plants were monosomic (Table 4). The data for chromosome 1A were
5 BAI ET AL. TRANSFER OF LEAF RUST RESISTANCE TO WHEAT 687 slightly equivocal. Six families had only disomic plants but two families each had three disomic plants and one monosomic, indicating that two of the plants could have been monosomic. However, in one case, the monosomic count was marked as questionable. It is concluded that both counts were incorrect and all eight plants were disomic. Thus 1A is the critical chromosome. DISCUSSION A gene giving good resistance to isolates of 10 races of leaf rust was transferred from T. timopheevii to both durum and bread wheat. In durum wheat, the gene was dominant but in bread wheat it behaved as a recessive. Apparently the D genome carries a gene or genes that modify the dominance of the gene for resistance. However, the effectiveness of the gene for resistance is basically unchanged the durum and bread wheat lines carrying the gene are only slightly less resistant than the T. timopheevii parents. In transfers of genes for rust resistance to bread wheat from its relatives, it is not uncommon for the resistance to be diminished (e.g., Dyck and Kerber 1970; Kerber and Dyck 1973). The gene should be valuable in both durum and bread wheat breeding. Monosomic analysis showed that the gene is on chromosome 1A, apparently the first time a gene for rust resistance from T. timopheevii has been located on an A-genome chromosome. Since chromosome locations for only five other genes for rust resistance have been reported, this may be just chance. However, it is also possible that more genes for rust resistance are located on the G-genome chromosomes than on the A-genome chromosomes. The only other named gene for leaf rust resistance derived from T. timopheevii is Lr18 on chromosome 5B. The leaf rust resistance transferred by Allard (1949) is presumably linked to Sr36 on chromosome 2B. The only named gene for leaf rust resistance on chromosome 1A is Lr10 (McIntosh et al. 1995). A Thatcher line carrying Lr10 was tested with four of the races to which the T. timopheevii gene is resistant and was susceptible to all four (unpublished data). Thus, the gene is not Lr10, although it could be an allele. However, Lr10 was reported to have originated in bread wheat and is present in many older Australian cultivars (McIntosh et al. 1995), and is unlikely to have been derived from T. timopheevii. At least two additional genes for leaf rust resistance were transferred from T. timopheevii to durum wheat. They condition only moderate resistance and not to all of the 10 races used in the tests. Consequently, they are less likely to be of value in wheat breeding. ACKNOWLEDGMENTS The authors are pleased to acknowledge the support of the Natural Sciences and Engineering Research Council of Canada. Allard, R. W A cytogenetic study dealing with the transfer of genes from Triticum timopheevii to common wheat by backcrossing. J. Agron. Res. 78: Dyck, P. L. and Kerber, E. R Inheritance in hexaploid wheat of adult plant leaf rust resistance derived from Aegilops squarrosa. Can. J. Genet. Cytol. 12: Kerber, E. R. and Dyck, P. L Inheritance of stem rust resistance transferred from diploid wheat (Triticum monococcum) to tetraploid and hexaploid wheat and chromosome location of the gene involved. Can. J. Genet. Cytol. 15: Kimber, G. and Sears, E. R Evolution in the genus Triticum and the origin of cultivated wheat. Pages in E.G. Heyne, ed. Wheat and wheat improvement. 2nd ed. ASA, Madison, WI. McIntosh, R. A Genetic and cytogenetic studies involving Lr18 for resistance to Puccinia recondita. Pages in S. Sakamoto, ed. Proceedings of the sixth international wheat genetics symposium. 28 November 3 December Plant Germplasm Institute, Kyoto, Japan. McIntosh, R. A. and Gyarfas, J Triticum timopheevii as a source of resistance to wheat stem rust. Z. Pflanzenzuct. 66: McIntosh, R. A., Wellings, C. R. and Park, R. F Wheat rusts: an atlas of resistance genes. CSIRO, Australia. 200 pp. Mujeeb-Kazi, A. and Miranda, J. L Enhanced resolution of somatic chromosome constructions as an aid to identifying intergeneric hybrids among some Triticeae. Cytologia 50: Snow, R Alcoholic hydrochloric acid-carmine as a stain for chromosomes in squash preparations. Stain Technol. 38: Stakman, E. C., Stewart, D. M. and Loegering, W. Q Identification of physiologic races of Puccinia graminis var. tritici. USDA, Washington, DC. Bull. E617 (Revised).
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