Published in Crop Sci 39:1692-1696 (1999)
© 1999 Crop Science Society of America
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Crop Science 39:1692-1696 (1999)
© 1999 Crop Science Society of America
CELL BIOLOGY & MOLECULAR GENETICS
Transfer of Wheat-Rye Translocation Chromosomes Conferring Resistance to Hessian Fly from Bread Wheat into Durum Wheat
B. Friebea,
R.G. Kynasta,
J.H. Hatchettb,
R.G. Searsc,
D.L. Wilsona and
B.S. Gilla
a Dep. of Plant Pathology, Wheat Genetics Resource Center, Plant Sciences Building, Throckmorton Hall, Kansas State Univ., Manhattan, KS 66506-5502 USA
b USDA-ARS, Dep. of Entomology, Waters Hall, Kansas State Univ., Manhattan, KS 66506-5502 USA
c Dep. of Agronomy, Plant Sciences Building, Throckmorton Hall, Kansas State Univ., Manhattan, KS 66506-5502 USA
friebe{at}ksu.edu
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ABSTRACT
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The Hessian fly, Mayetiola destructor (Say), is a damaging pest of bread wheat, Triticum aestivum L., and durum wheat, T. turgidum L. ssp. durum Desf. Husn., in many wheat production areas of the world. Breeding for host plant resistance is the most agronomically desirable way to control this pest. Twenty-seven major genes conferring resistance to Hessian fly have been identified and used in wheat improvement. These genes confer resistance to specific biotypes of the Hessian fly. Recently, new sources of Hessian fly resistance derived from cultivated rye, Secale cereale L., have been reported that confer resistance to all known biotypes of the Hessian fly. The resistance gene H21 is present on the wheat-rye whole arm translocation T2BS·2R#2L. H25 is present on an interstitial rye segment in the 4AL arm of the wheat-rye translocation chromosome Ti4AS·4AL-6R#1L-4AL. The objective of the present study was to transfer H21 and H25 to tetraploid durum wheat, thereby making these genes available for the improvement of durum wheat. Homozygous T2BS·2R#2L and Ti4AS·4AL-6R#1L-4AL translocation durum lines were recovered that expressed the H21 and H25 resistance. The H25 durum translocation line was vigorous and set seeds similar to the durum wheat parental cultivar. Thus, the H25 transfer can be used directly in durum wheat improvement. Plant vigor and seed set of the H21 durum translocation line was drastically reduced, indicating that the missing 2BL arm in this translocation has genes that are essential for normal plant vigor and fertility. Further chromosome engineering is required to shorten the rye segment in this translocation before H21 can be used in durum breeding.
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INTRODUCTION
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THE HESSIAN FLY
is a destructive pest of bread wheat (T. aestivum L., 2n = 6x = 42, AABBDD) and durum wheat T. turgidum L. ssp. durum Desf. Husn., 2n = 4x = 28, AABB) in most production areas of the world. To date, 29 major genes conferring resistance to Hessian fly have been identified and are being used in cultivar improvement (McIntosh et al., 1998). Most of these genes confer resistance only against specific biotypes of the Hessian fly.
Cultivated rye (S. cereale L., 2n = 2x = 14, RR) is an important source of genes for insect and disease resistance in wheat. To date, 12 genes conferring resistance to various diseases and insects have been transferred from rye into wheat (Friebe et al., 1996). The designated genes include those conferring resistance to leaf rust, caused by Puccinia recondita f. sp. tritici Rob. ex Desm. (Lr25, Lr26, Lr45); stripe rust, caused by P. striiformis f. sp. tritici Westend. (Yr9); stem rust, caused by P. graminis f. sp. tritici Eriks. & Henn. (Sr27, Sr31); powdery mildew, caused by Blumeria graminis f. sp. tritici DC. E. O. Speer (Pm7, Pm8, Pm17, Pm20), greenbug (Schizaphis graminum Rond.) (Gb2, Gb6), and Hessian fly (H21, H25). Some of these genes are being used in cultivar improvement (Friebe et al., 1996).
Genes H21 and H25 confer resistance to biotypes Great Plains `GP' and biotypes A through L of the Hessian fly (Friebe et al., 1990, 1991; Mukai et al., 1993; Ratcliffe and Hatchett, 1997). H21 was derived from the rye cultivar Chaupon and was transferred to bread wheat via a wheat-rye translocation that apparently was induced by tissue culture of a wheat-rye hybrid. The resistance gene H25 was derived from the rye cultivar Balbo and was transferred to wheat by radiation treatment.
The Hessian fly causes severe damage, especially in the main durum wheat producing areas in the Mediterranean and in North Africa. By screening thousands of accessions of durum wheat, only one source of resistance to Hessian fly was identified in a recent survey carried out in Morocco (Nsarellah et al., 1998). Average annual losses in grain yield caused by Hessian fly were estimated to 32% but severe Hessian fly infestation may result in total crop failure (Lhaloui et al., 1992; Nsarellah et al., 1998). At least in North Africa, H21 and H25 confer resistance to the prevalent biotypes of the Hessian fly (El Bouhssini et al., 1996). Thus, there is an interest in deploying genes such as H21 and H25 for improving durum wheat. The present study reports the transfer of H21 and H25 durum wheat improvement.
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Material and methods
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The durum parent was the North American cultivar Cando, which was kindly provided by Dr. L.R. Joppa USDA-ARS, North Dakota State University, Fargo. The hard red winter wheat germplasm PI 549276, Hamlet (ND7532/Chaupon//4*ND7532) is the source of the Hessian fly resistance gene H21. H21 is located on the long arm rye chromosome 2R#2, which is present in PI 549276 in the form of a compensating whole arm translocation T2BS·2R#2L (Sears et al., 1992). The hard red winter wheat germplasm KS92WGRC20, PI 592732 (TAM-101/4/Suwon92/Balbo rye//TAM-106/3/Amigo) (Sebesta et al., 1997) is the source of H25. H25 is located on a 0.7-µm long rye segment derived from the distal region of rye chromosome arm 6R#1L inserted into the long arm of wheat chromosome 4A in form of an interstitial Ti4AS·4AL-6R#1L-4AL wheat-rye translocation.
Chromosome identification was based on the standard karyotypes of wheat (Gill and Kimber, 1974a) and rye (Gill and Kimber, 1974b; Mukai et al., 1992) and was determined by the standard C-banding protocol described by Gill et al. (1991). Genomic in situ hybridization (GISH) analysis was according to Jiang et al. (1994). The resistance evaluations were according to Hatchett et al. (1981) and Friebe et al. (1990). Plants in the seedling stage were evaluated for their reaction to biotype L of the Hessian fly. Biotype L is the most virulent biotype presently found in North America. The larvae can infest wheat with H1 through H8, H11, and H15, but not wheat with H9, H10, H12, H13, H14, or H16 through H19. To determine the seed set after self-pollination, the number of seeds per spikelet was determined in five spikes per line.
Cando was crossed as a female with PI 549276 and KS92WGRC20 and the F1 was backcrossed as male and female to Cando. Plants heterozygous for the wheat-rye translocations in the BC1F1 through BC3F1 were identified by C-banding. Plants homozygous for the wheat-rye translocations were recovered in the BC2F2 and BC3F2 generations, and their progenies were evaluated for their reaction to biotype L of the Hessian fly.
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Results
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Transfer of H21 into Durum Wheat
The crosses Cando/PI 549276 and Cando/KS92WGRC20 produced 4 and 10 seeds, respectively. Half of the F1 seeds were grown in the spring in a greenhouse. All plants had 2n = 35 chromosomes but died as seedlings (Table 1)
. The remaining F1 seeds were grown in the greenhouse in the fall. Under cooler growing conditions, the plants with 2n = 35 chromosomes flowered and were backcrossed as males and females with Cando.
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Table 1 Pedigrees, chromosome numbers, and status of the wheat-rye translocation chromosome T1BL · 2R#2L in in backcross derivatives of the durum wheat cultivar Cando with the T. aestivum PI 549276, the source of the Hessian fly resistance gene H21
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Five BC1F1 seeds from the cross Cando//Cando/PI 549276 were grown, which had 2n = 30 (1), 31 (1), 33 (2), and 34 (1) chromosomes and three of them were heterozygous for T2BS·2R#2L. Twelve BC1F1 seeds from the reciprocal cross Cando/PI 549276//Cando were grown, which had 2n = 30 (1), 31 (2), 32 (3), 33 (4), and an unknown number of chromosomes (2). Only one of these plants was heterozygous for T2BS·2R#2L. All BC1F1 plants heterozygous for T2BS·2R#2L had severe, multi-branched spike deformations and were crossed with Cando as males and females. The BC2F1 seeds were plump and white when Cando was used as female and usually red and shriveled when Cando was used as male parent.
All 12 BC2F1 progenies obtained from the backcross with Cando as female were disomic for chromosome 2B, while among 17 progenies obtained with Cando as male, with 2n = 28 (11) and 29 (6) chromosomes, six were heterozygous for T2BS·2R#2L. Plants heterozygous for T2BS·2R#2L had no spike deformations and were backcrossed as males with Cando and also selfed. All BC2F2-derived seeds were plump and white and sixteen were grown and analyzed cytologically. All plants had 2n = 28 chromosomes; three were homozygous for T2BS·2R#2L, five were disomic for 2B, and eight were heterozygous for T2BS·2R#2L. Although the heterozygous plants were vigorous and fertile, the plant homozygous for T2BS·2R#2L were very weak and completely male sterile. Thus, plants heterozygous for T2BS·2R#2L were backcrossed as males to Cando. Eight of the BC3F1 seeds were grown and three were heterozygous for T2BS·2R#2L and these plants were selfed.
The BC3F2 seeds were plump and white. Twenty-one plants with 2n = 28 chromosomes were grown; four were homozygous for T2BS·2R#2L (Fig. 1a)
, seven were disomic for 2B, and 11 were heterozygous. The heterozygous plants again were more vigorous and set on average 2.5 seeds per spikelet, which is similar to the recipient durum wheat parent Cando that produced on average 2.2 seeds per spikelet. One of the three homozygous T2BS·2R#2L plants was male sterile, whereas the remaining two plants set on average 1.2 and 0.4 seeds per spikelet. The spikes of the plants homozygous for T2BS·2R#2L were smaller than the durum parent Cando (Fig. 2)
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Fig. 1 Genomic in situ hybridization patterns of mitotic metaphase chromosomes of T1BL·2R#2L (a) and Ti4AS·4AL-6R#1L-4AL (b) durum wheat germplasms. Rye chromatin is visualized by yellow FITC fluorescence whereas wheat chromatin is counterstained with propidium iodide and fluoresce red
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Fig. 2 Spike morphologies of the recipient durum wheat cultivar Cando (left), the Ti4AS·4AL-6R#1L-4AL durum wheat germplasms (middle), and the T1BL·2R#2L durum wheat germplasm (right)
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Homozygous T2BS·2R#2L BC3F3 plants were screened for their reaction to the Hessian fly biotype L. All 18 T2BS·2R#2L BC2F3 plants and nine plants of the H21 donor germplasm PI 549276 were resistant and larvae died, whereas all the 36 plants of the recipient durum cultivar Cando were susceptible and had live larvae.
Transfer of H25 into Durum Wheat
Nine BC1F1 seeds from the cross Cando//Cando/KS92WGRC20 were grown, which had 2n = 29 (1), 30 (4), 31 (2), and 33 (2) chromosomes (Table 2)
and four of them were heterozygous for Ti4AS·4AL-6R#1L-4AL. Ten BC1F1 seeds from the reciprocal cross Cando/KS92WGRC20//Cando were grown and four of them were heterozygous for Ti4AS·4AL-6R#1L-4AL, with 2n = 28 (2), 30 (1), and 31 (1) chromosomes. The majority of the plants heterozygous for Ti4AS·4AL-6R#1L-4AL had no spike deformation. No BC2F1 seeds were obtained when Cando was used as female parent, and all BC2F1 seeds from the reciprocal cross were red and shriveled but germinated.
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Table 2 Pedigrees, chromosome numbers, and status of the wheat-rye translocation chromosome Ti4AS·4AL-6R#1L-4AL in backcross derivatives of the durum wheat cultivar Cando with the T. aestivum germplasm KS29WGRC20, the source of the Hessian fly resistance gene H25
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Five BC2F1 plants were obtained, which had 2n = 28 (3) and 29 (2) chromosomes and two of them were heterozygous for Ti4AS·4AL-6R#1L-4AL. These plants had normal spike morphology and were selfed. All BC2F2 seeds were plump and white and the chromosomal constitution was determined in 11 of them. All had 2n = 28 chromosomes; three plants were homozygous for Ti4AS·4AL-6R#1L-4AL (Fig. 1b), three were disomic for wheat chromosome 4A, and five plants were heterozygous for Ti4AS·4AL-6R#1L-4AL.
Homozygous Ti4AS·4AL-6R#1L-4AL BC2F3 plants were vigorous and set on average 2.4 seeds per spikelet after self-pollination, which is similar to the seed set of the durum cultivar Cando. Spike morphology of the homozygous Ti4AS·4AL-6R#1L-4AL translocation line is similar to that of the durum wheat parent Cando, but the awns are more widely spread (Fig. 2).
Thirty-six of the homozygous Ti4AS·4AL-6R#1L-4AL BC2F3 plants together with 17 plants of the H25 donor germplasm PI 592732 were evaluated for their resistance to the Hessian fly biotype L with the recipient durum cultivar Cando as a control. All the 58 Cando plants tested were susceptible with live larvae whereas all 36 durum wheat plants homozygous Ti4AS·4AL-6R#1L-4AL and the 17 plants of PI 592732 were resistant. All the resistant plants had dead larvae indicating that there were no escapes.
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Discussion
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Wild relatives and related species are important sources for disease and pest resistance of cultivated bread wheat. A large number of agronomically useful alien genes have been transferred to hexaploid wheat, mainly by irradiation and induced homoeologous recombination. However, only a few of them have contributed to cultivar improvement because of the non-compensating nature of the transfers (Friebe et al., 1996).
The most successful wheat-alien transfers are the wheat-rye whole arm translocations T1BL·1R#1S and T1AL·1R#2S, which are still used worldwide in wheat improvement (Lukaszewski, 1990). The 1RS arm has genes conferring resistance to leaf rust, Lr26; stripe rust, Yr9; stem rust, Sr31; powdery mildew, Pm8 and Pm17; and greenbug, Gb2 (Gb6 is present on T1AL·1R#3S) (Friebe et al., 1996). The 1RS arm in these translocations not only compensates for the loss of wheat chromosome arms 1BS and 1AS, but in some genetic backgrounds also has a heterotic effect on grain yield (Villareal et al., 1991, 1995; McKendry et al., 1996; Singh et al., 1998). RFLP analysis showed that chromosome 1R is the only rye chromosome that is not structurally rearranged compared with the homoeologous groups of wheat (Devos et al., 1993).
So far, only a few wheat-alien translocations have been transferred to durum wheat. Rao (1978) introduced stem rust resistance derived from rye and Agropyron elongatum (Host.) P. Beauv. into durum wheat. The wheat-alien translocation chromosomes had no transmission through the pollen, and homozygous translocation lines were not recovered. Friebe et al. (1987, 1993), William and Mujeeb-Kazi (1993), and Mujeeb-Kazi et al. (1996) transferred the T1BL·1R#1S translocation to durum wheat. Homozygous translocation germplasm lines with normal plant vigor and seed set were recovered. Ceoloni et al. (1996) transferred Pm13, derived from Aegilops longissima chromosome 3Sl#1, to the short arm of wheat chromosome 3B of bread and durum wheat. The T3BL·3BS-3Sl#1S translocation has normal male and female transmission in durum wheat. Ceoloni et al. (1996) also transferred the T7AS-7Ae#1·S7Ae#1L wheat-Agropyron elongatum translocation (transfer No. 12, Sears, 1973) with the leaf rust resistance gene Lr19 to durum wheat. However, the lack of male transmission prevented the recovery of homozygous translocation stocks.
In the present study, durum wheat germplasm lines homozygous for the T2BS·2R#2L and Ti4AS·4AL-6R#1L-4AL translocations were recovered that express H21 and H25 resistance to Hessian fly, respectively. Spike abnormalities present in earlier backcross generations were not observed in the homozygous translocation lines. The T2BS·2R#2L translocation chromosome was not transmitted through the pollen in BC1F1 plants, but similar to the Ti4AS·4AL-6R#1L-4AL translocation, had normal male and female transmission in the BC2 and BC3. The Ti4AS·4AL-6R#1L-4AL translocation stock is as vigorous as the recipient durum wheat cultivar and has a similar seed set. The H25 resistant Ti4AS·4AL-6R#1L-4AL durum wheat germplasm can be used directly in breeding programs.
Plants heterozygous for T2BS·2R#2L have plant vigor and seed set similar to the durum wheat parent. Homozygous T2BS·2R#2L plants are less vigorous and set fewer seed. RFLP analysis indicated that the 2RL arm is not structurally rearranged compared with group 2 long arms of wheat (Devos et al., 1993). The 2RL arm in T2BS·2R#2L is expected to compensate well for the loss of wheat chromosome arm 2B. The T2BS·2R#2L translocation at the hexaploid level has no negative effect on plant vigor; however, it drastically reduces vigor and seed set at the tetraploid durum wheat level. Further chromosome engineering is required to shorten the rye segment in T2BS·2R#2L before H21 can be exploited for durum wheat improvement.
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ACKNOWLEDGMENTS
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This work was supported by a United States Department of Agriculture, Cooperative State Research Service special grant to the Wheat Genetics Research Center at Kansas State University, Manhattan, Kansas, and a by a grant from the Kansas Wheat Commission. Contribution No. 99-258-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, KS 66506-5502.
Received for publication December 15, 1998.
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ABSTRACT
INTRODUCTION
