Abstract
Key message
Twenty-two compensating wheat-Dasypyrum villosum translocations carrying the powdery mildew resistance gene PmV were developed using a triple marker selection strategy in a large homozygous ph1bph1b population.
Abstract
Powdery mildew, caused by Blumeria graminis f. sp. tritici (Bgt), is a destructive wheat disease in China. Currently, nearly all resistant varieties grown in the middle and lower reaches of the Yangtze River carry Pm21 which is present in a wheat-Dasypyrum villosum T6V#2S·6AL translocation. Its widespread use poses a strong risk of loss of effectiveness if the pathogen were to change. PmV, a Pm21 homolog carried by a wheat-D. villosum T6V#4S·6DL translocation, is also resistant to powdery mildew but is less transmittable and exploited in cultivars. To utilize PmV more effectively, a new recombinant translocation T6V#4S-6V#2S·6AL carrying PmV with a higher transmission rate was used as a basic material for inducing smaller alien translocations. A locally adapted ph1b-carrying line, Yangmai 23-ph1b, was crossed with T6V#4S-6V#2S·6AL to generate a homozygous ph1bph1b population of 6300 F3 individuals. A modified triple marker strategy based on three co-dominant markers including the functional marker MBH1 for PmV in combination with distal and proximal markers 6VS-GX4 and 6VS-GX17, respectively, was used to screen for new recombinants efficiently. Forty-eight compensating translocations were identified, 22 of which carried PmV. Two translocation lines, Dv6T25 with the shortest distal segment carrying PmV and Dv6T31 with the shortest proximal segment carrying PmV were identified, both expressed normal transmission and therefore could promote PmV in wheat breeding. This work exemplifies a model for rapid development of wheat-alien compensating translocations.
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All the data generated or analyzed in this study are available in the manuscript and the supplementary information.
References
Bhullar R, Nagarajan R, Bennypaul H, Sidhu G, Sidhu G, Rustgi S, von Wettstein D, Gill K (2014) Silencing of a metaphase I-specific gene results in a phenotype similar to that of the Pairing homeologous 1 (Ph1) gene mutations. Proc Natl Acad Sci 111:14187–14192
Bie T, Cao Y, Chen P (2007) Mass production of intergeneric chromosomal translocations through pollen irradiation of Triticum durum-Haynaldia villosa amphiploid. J Intergr Plant Biol 49:1619–1626
Bie T, Zhao R, Zhu S, Chen S, Cen B, Zhang B, Gao D, Jiang Z, Chen T, Wang L et al (2015a) Development and characterization of marker MBH1 simultaneously tagging genes Pm21 and PmV conferring resistance to powdery mildew in wheat. Mol Breed 35:189
Bie T, Zhao R, Jiang Z, Gao D, Zhang B, He H (2015b) Efficient marker-assisted screening of structural changes involving Haynaldia villosa chromosome 6V using a double-distal-marker strategy. Mol Breed 35:34
Chen P, Qi L, Zhou B, Zhang S, Liu D (1995) Development and molecular cytogenetic analysis of wheat-Haynaldia villosa 6VS/6AL translocation lines specifying resistance to powdery mildew. Theor Appl Genet 91:1125–1128
Chen X, Shi A, Shang L, Steven L, Jpaul M (1997) The resistance reaction of H. villosa to powdery mildew isolates and its expression in wheat background. Acta Phytopath Sin 27:17–22 (in Chinese with English abstract)
Chen S, Chen P, Wang X (2008) Inducement of chromosome translocation with small alien segments by irradiating mature female gametes of the whole arm translocation line. Sci China Ser C 51:346–352
Chen P, You C, Hu Y, Chen S, Zhou B, Cao A, Wang X (2013) Radiation-induced translocations with reduced Haynaldia villosa chromatin at the Pm21 locus for powdery mildew resistance in wheat. Mol Breed 31:477–484
Friebe B, Qi L, Liu C, Liu W, Gill B (2012) Registration of a hard red winter wheat genetic stock homozygous for ph1b for facilitating alien introgression for crop improvement. J Plant Regist 6:121
Gill B (1991) Standard karyotype and system for description of chromosome bands and structural aberrations in wheat. Genome 34:830–839
He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qiu D, Li H, Bie T (2018) Pm21, encoding a typical CC-NBS-LRR protein, confers broad-spectrum resistance to wheat powdery mildew disease. Mol Plant 11:879–882
Li H, Chen X, Xin Z, Ma Y, Xu H, Chen X, Jia X (2005) Development and identification of wheat-Haynaldia villosa T6DL.6VS chromosome translocation lines conferring resistance to powdery mildew. Plant Breed 124:203–205
Li S, Jia Z, Wang K, Du L, Li H, Lin Z, Ye X (2020a) Screening and functional characterization of candidate resistance genes to powdery mildew from Dasypyrum villosum#4 in a wheat line Pm97033. Theor Appl Genet 133:3067–3083
Li Y, Li Q, Li Y, Lan J, Tang H, Qi P, Ma J, Wang J, Chen G, Pu Z et al (2020b) Transfer of the ph1b gene of ‘Chinese Spring’ into a common wheat cultivar with excellent traits. Cereal Res Commun 48:283–291
Li H (2010) Inducing chromosomal translocations between wheat and Haynaldia villosa through using Chinese Spring ph1b mutant and Tal-PhI genetic stock. Doctoral dissertation, Nanjing Agricultural University
Lukaszewski A, Cowger C (2017) Re-engineering of the Pm21 transfer from Haynaldia villosa to bread wheat by induced homoeologous recombination. Crop Sci 57:2590–2594
Lukaszewski A, Rybka K, Korzun V, Malyshev S, Lapinski B, Whitkus R (2004) Genetic and physical mapping of homoeologous recombination points involving wheat chromosome 2B and rye chromosome 2R. Genome 47:36–45
Ma X, Chang Y, Chen J, Yu M, Wang B, Ye X, Lin Z (2022) Development of wheat-Dasypyrum villosum T6V#4S·6AL translocation lines with enhanced inheritance for powdery mildew resistance. Theor Appl Genet 135:2423–2435
Mukai Y, Gill B (1991) Detection of barley chromatin added to wheat by genomic in situ hybridization. Genome 34:448–452
Mukai Y, Nakahara Y, Yamamoto M (1993) Simultaneous discrimination of the three genomes in hexaploid wheat by multicolor fluorescence in situ hybridization using total genomic and highly repeated DNA probes. Genome 36:489–494
Rey M, Calder N, Prieto P (2015) The use of the ph1b mutant to induce recombination between the chromosomes of wheat and barley. Front Plant Sci 6:160
Sears E (1976) Genetic control of chromosome pairing in wheat. Annu Rev Genet 10:31–51
Sears E (1981) Transfer of alien genetic material to wheat. In: Evans LT, Peacock WL (eds) Wheat science: today and tomorrow. Cambridge University Press, Cambridge, pp 75–89
Türkösi E, Ivanizs L, Farkas A, Gaál E, Kruppa K, Kovács P, Szakács É, Szőke K, Said M, Cápal P et al (2022) Transfer of the ph1b deletion chromosome 5B from Chinese Spring wheat into a winter wheat line and induction of chromosome rearrangements in wheat-Aegilops biuncialis hybrids. Front Plant Sci 13:875676
Wan W, Xiao J, Li M, Tang X, Wen M, Cheruiyot A, Li Y, Wang H, Wang X (2020) Fine mapping of wheat powdery mildew resistance gene Pm6 using 2B/2G homoeologous recombinants induced by the ph1b mutant. Theor Appl Genet 133:1265–1275
Wang X, Lai J, Chen L, Liu G (1998) Molecular identification for Chinese Spring ph1b mutant. Sci Agric Sin 31:31–34 (in Chinese with English abstract)
Wang B, Ma X, Ye X, Zhou Y, Ma Y, Lin Z (2021) Genotypic and phenotypic characterization of two Triticum aestivum L.-Dasypyrum villosum translocations lines in the same wheat genetic background. Agronomy 11:399
Wu N, Lei Y, Pei D, Wu H, Liu X, Fang J, Guo J, Wang C, Guo J, Zhang J et al (2021) Predominant wheat-alien chromosome translocations in newly developed wheat of China. Mol Breed 41:1–16
Xing L, Hu P, Liu J, Witek K, Zhou S, Xu J, Zhou W, Gao L, Huang Z, Zhang R et al (2018) Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol Plant 11:874–878
Zhang X, Wan W, Li M, Yu Z, Liu J, Holuová K, Vrána J, Doleel J, Wu Y, Wang H (2021) Targeted sequencing of the short arm of chromosome 6V of a wheat relative Haynaldia villosa for marker development and gene mining. Agronomy 11:1695
Zhang X, Wang H, Sun H, Li Y, Feng Y, Jiao C, Li M, Song X, Wang T, Wang Z et al (2023) A chromosome-scale genome assembly of Dasypyrum villosum provides insights into its application as a broad-spectrum disease resistance resource for wheat improvement. Mol Plant 16:432–451
Zhao R, Wang H, Xiao J, Bie T, Cheng S, Jia Q, Yuan C, Zhang R, Cao A, Chen P et al (2013) Induction of 4VS chromosome recombinants using the CS ph1b mutant and mapping of the wheat yellow mosaic virus resistance gene from Haynaldia villosa. Theor Appl Genet 126:2921–2930
Zhao R, Liu B, Jiang Z, Chen T, Wang L, Ji Y, Hu Z, He H, Bie T (2019) Comparative analysis of genetic effects of wheat-Dasypyrum villosum translocations T6V#2S·6AL and T6V#4S·6DL. Plant Breed 138:503–512
Acknowledgments
The authors are grateful to Prof. Xiao Chen (Institute of Crop Sciences, Chinese Academy of Agricultural Sciences) for providing the T6V#4S·6DL translocation line. We are also grateful to Dr. Robert Alexander McIntosh (University of Sydney, Australia) for kindly revising the manuscript.
Funding
This research was supported by the grants from the National Natural Science Foundation of China (32072065 and 32201808), Natural Science Foundation in Jiangsu Province (BK20201217), Seed Industry Revitalization Project in Jiangsu Province [JBGS(2021)006], and the Key Project for Research and Development in Jiangsu Province (BE2022346).
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TB, WW, RZ conceived and designed the experiments. RZ, TC, and LW performed genotyping of the population. WW, RZ, and HL performed physical identification of the candidate translocations. XZ and XW supported genomic information and assisted sequence analysis. WW, RZ, and TB wrote the manuscript. All authors read and approved the final manuscript.
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Communicated by Steven S. Xu.
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Workflow for development of Yangmai 23-ph1b
Supplementary file1 (PNG 202 KB)
122_2023_4393_MOESM2_ESM.png
Recombination models of compensating translocations detected by the triple marker strategy. Characters A, B and H represent homozygous marker allele A, homozygous marker allele B and heterozygous, respectively. The order of markers is 6VS-GX4 - MBH1 - 6VS-GX17. Genotypes “A-A-A”, “B-B-B” and “H-H-H”, plants without recombination. The other combinations are putative recombinants
Supplementary file2 (PNG 233 KB)
122_2023_4393_MOESM3_ESM.png
Powdery mildew responses of the newly developed wheat-D. villosum compensating translocations. Yangmai 22, resistant control; Yangmai 23, susceptible control; Dv6T01-Dv6T48, compensating translocations
Supplementary file3 (PNG 7181 KB)
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Wan, W., Zhao, R., Chen, T. et al. Rapid development of wheat-Dasypyrum villosum compensating translocations resistant to powdery mildew using a triple marker strategy conducted on a large ph1b-induced population. Theor Appl Genet 136, 148 (2023). https://doi.org/10.1007/s00122-023-04393-z
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DOI: https://doi.org/10.1007/s00122-023-04393-z