Abstract
Key message
We developed T1AL·1PS and T1AS·1PL Robertsonian translocations by breakage-fusion mechanism based on wheat-A. cristatum 1P(1A) substitution line with smaller leaf area, shorter plant height, and other excellent agronomic traits
Abstract
Agropyron cristatum, a wild relative of wheat, is a valuable germplasm resource for improving wheat genetic diversity and yield. Our previous study confirmed that the A. cristatum chromosome 1P carries alien genes that reduce plant height and leaf size in wheat. Here, we developed T1AL·1PS and T1AS·1PL Robertsonian translocations (RobTs) by breakage-fusion mechanism based on wheat-A. cristatum 1P (1A) substitution line II-3-1c. Combining molecular markers and cytological analysis, we identified 16 spontaneous RobTs from 911 F2 individuals derived from the cross of Jimai22 and II-3-1c. Fluorescence in situ hybridization (FISH) was applied to detect the fusion structures of the centromeres in wheat and A. cristatum chromosomes. Resequencing results indicated that the chromosomal junction point was located at the physical position of Triticum aestivum chromosome 1A (212.5 Mb) and A. cristatum chromosome 1P (230 Mb). Genomic in situ hybridization (GISH) in pollen mother cells showed that the produced translocation lines could form stable ring bivalent. Introducing chromosome 1PS translocation fragment into wheat significantly increased the number of fertile tillers, grain number per spike, and grain weight and reduced the flag leaf area. However, introducing chromosome 1PL translocation fragment into wheat significantly reduced flag leaf area and plant height with a negative effect on yield components. The pre-breeding of two spontaneous RobTs T1AL·1PS and T1AS·1PL was important for wheat architecture improvement.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data and materials supporting the current study can be obtained by contacting the corresponding authors.
Code availability
Not applicable.
References
Ardalani S, Mirzaghaderi G, Badakhshan H (2016) A Robertsonian translocation from Thinopyrum bessarabicum into bread wheat confers high iron and zinc contents. Plant Breed 135:286–290. https://doi.org/10.1111/pbr.12359
Bohra A, Kilian B, Sivasankar S, Caccamo M, Mba C, McCouch SR, Varshney RK (2022) Reap the crop wild relatives for breeding future crops. Trends Biotechnol 40(4):412–431. https://doi.org/10.1016/j.tibtech.2021.08.009
Cai X, Jones SS, Murray TD (1998) Molecular cytogenetic characterization of thinopyrum and wheat-Thinopyrum translocated chromosomes in a wheat-Thinopyrum amphiploid. Chromosome Res 6:183–189. https://doi.org/10.1023/A:1009255516850
Cao Y, Zhong Z, Wang H, Shen R (2022) Leaf angle: a target of genetic improvement in cereal crops tailored for high-density planting. Plant Biotechnol J 20(3):426–436. https://doi.org/10.1111/pbi.13780
Coombes B, Fellers JP, Grewal S, Rusholme-Pilcher R, Hubbart-Edwards S, Yang CY, Joynson R, King IP, King J, Hall A (2023) Whole-genome sequencing uncovers the structural and transcriptomic landscape of hexaploid wheat/Ambylopyrum muticum introgression lines. Plant Biotechnol 21(3):482–496. https://doi.org/10.1111/pbi.13859
Danilova TV, Friebe B, Gill BS, Poland J, Jackson E (2018) Development of a complete set of wheat-barley group-7 Robertsonian translocation chromosomes conferring an increased content of β-glucan. Theor Appl Genet 131:377–388. https://doi.org/10.1007/s00122-017-3008-z
Dong YS, Zhou RH, Xu SJ, Li LH, Caudero Y, Wang RC (1992) Desirable characteristics in perennial triticeae collected in china for wheat improvement. Hereditas 116:176–178. https://doi.org/10.1111/j.1601-5223.1992.tb00224.x
Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays l.). Adv Agron 86:83–145. https://doi.org/10.1016/S0065-2113(05)86002-X
Faris JD, Xu SS, Cai X, Friesen TL, Jin Y (2008) Molecular and cytogenetic characterization of a durum wheat-Aegilops speltoides chromosome translocation conferring resistance to stem rust. Chromosome Res 16:1097–1105. https://doi.org/10.1007/s10577-008-1261-3
Friebe B, Jiang J, Raupp WJ, Mcintosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91:59–87. https://doi.org/10.1007/BF00035277
Friebe B, Zhang P, Linc G, Gill BS (2005) Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase i and rejoining of broken centromeres during interkinesis of meiosis ii. Cytogenet Genome Res 109:293–297. https://doi.org/10.1159/000082412
Fu S, Chen L, Wang Y, Li M, Tang Z (2015) Oligonucleotide probes for nd-fish analysis to identify rye and wheat chromosomes. Sci Rep 5:10552. https://doi.org/10.1038/srep10552
Ghazali S, Mirzaghaderi G, Majdi M (2015) Production of a novel Robertsonian translocation from Thinopyrum bessarabicum into bread wheat. Tsitol 49:38–42. https://doi.org/10.3103/S0095452715060031
Grewal S, Edwards SH, Yang CY, King, (2020) Rapid identification of homozygosity and site of wild relative introgressions in wheat through chromosome-specific kasp genotyping assays. Plant Biotechnol J. https://doi.org/10.1111/pbi.13241
Han F, Lamb JC, Birchler JA (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Natl Acad Sci USA 103:3238–3243. https://doi.org/10.1073/pnas.0509650103
Han H, Liu W, Lu Y, Zhang J, Yang X, Li X, Hu Z, Li L (2017) Isolation and application of P genome-specific DNA sequences of Agropyron Gaertn. in Triticeae. Planta 245:425–437. https://doi.org/10.1007/s00425-016-2616-1
Iwgsc IWGSC, Bellec A, Berges H, Vautrin S, Alaux M, Alfama F et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. https://doi.org/10.1126/science.aar7191
Jagannath DR, Bhatia CR (1972) Effect of rye chromosome 2 substitution on kernel protein content of wheat. Theor Appl Genet 42:89–92. https://doi.org/10.1007/bf00277949
Jauhar P (2006) Cytological analyses of hybrids and derivatives of hybrids between durum wheat and Thinopyrum bessarabicum, using multicolour fluorescent GISH. Plant Breed 125:19–26. https://doi.org/10.1111/j.1439-0523.2006.01176.x
Jiang J, Gill BS (1993) Sequential chromosome banding and in situ hybridization analysis. Genome 36(4):792–795. https://doi.org/10.1139/g93-104
King J, Grewal S, Yang CY, Hubbart S, Scholefield D, Ashling S et al (2017) A step change in the transfer of interspecific variation into wheat from Amblyopyrum muticum. Plant Biotechnol J. https://doi.org/10.1111/pbi.12606
King J, Grewal S, Fellers JP, King IP (2022) Exploring untapped wheat genetic resources to boost food security. In: Reynolds MP, Braun HJ (eds) Wheat improvement: food security in a changing climate. Springer, Cham, pp 3–15
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al (2009) The sequence alignment/ map format and samtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li G, Zhang T, Yu Z, Wang H, Yang E, Yang Z (2021) An efficient Oligo-FISH painting system for revealing chromosome rearrangements and polyploidization in Triticeae. Plant J 105:978–993. https://doi.org/10.1111/tpj.15081
Li H, Dong Z, Ma C, Xia Q, Tian X, Sehgal S, Koo DH, Friebe B, Ma P, Liu W (2020) A spontaneous wheat-Aegilops longissima translocation carrying Pm66 confers resistance to powdery mildew. Theor Appl Genet 133:1149–1159. https://doi.org/10.1007/s00122-020-03538-8
Li H, Zhou Y, Xin W, Wei Y, Guo ZJ, L, (2019) Wheat breeding in northern China: achievements and technical advances. Crop J 7:718–729. https://doi.org/10.1016/j.cj.2019.09.003
Li L, Dong Y, Zhou R, Li X, Pei L (1995) Cytogenetics and self -fertility of hybrids between Triticum aestivum L. and Agropyron cristatum (L.) Gaertn. Acta Genet Sin 22:109–114
Li YW, Li HJ, Liang H, Tang SX, Jia X (2000) Fluorescence in situ hybridization applied to the meiotic analysis and spontaneous chromosome translocation in the pollen mother cells of hybrids of Triticum-Haynaldia. Acta Genet Sin 27:317–324
Liu C, Qi L, Liu W, Zhao W, Wilson J, Friebe B, Gill BS (2011a) Development of a set of compensating Triticum aestivum-Dasypyrum villosum Robertsonian translocation lines. Genome 54(10):836–844. https://doi.org/10.1139/g11-05
Liu W, Jin Y, Rouse M, Friebe B, Gill B, Pumphrey MO (2011b) Development and characterization of wheat-Ae. searsii Robertsonian translocations and a recombinant chromosome conferring resistance to stem rust. Theor Appl Genet 122:1537–1545. https://doi.org/10.1007/s00122-011-1553-4
Liu W, Koo DH, Friebe B, Gill BS (2016) A set of Triticum aestivum-Aegilops speltoides Robertsonian translocation lines. Theor Appl Genet 129:2359–2368. https://doi.org/10.1007/s00122-016-2774-3
Lukaszewski AJ (1990) Frequency of 1RS/1AL and 1RS/1BL translocations in the United States wheats. Crop Sci 30:1151–1153. https://doi.org/10.2135/cropsci1990.0011183X003000050041x
Lukaszewski AJ (1993) Reconstruction in wheat of complete chromosomes 1B and 1R from the 1RS.1BL translocation of ‘kavkaz’ origin. Genome 36:821–824. https://doi.org/10.1139/g93-109
May CE, Appels R (1978) Rye chromosome 2R substitution and translocation lines in hexaploid wheat. Cereal Res. Commun. 6(3):231–234
Megyeri M, Molnár-Láng M, Molnár I (2013) Cytomolecular identification of individual wheat-wheat chromosome arm associations in wheat-rye hybrids. Cytogenet Genome Res 139:128–136. https://doi.org/10.1159/000346047
Mottaleb KA, Kruseman G, Frija A, Sonder K, Lopez-Ridaura S (2023) Projecting wheat demand in China and India for 2030 and 2050: implications for food security. Front Nutr 9:1077443. https://doi.org/10.3389/fnut.2022.1077443
Pan C, Li Q, Lu Y, Zhang J, Liu W (2017) Chromosomal localization of genes conferring desirable agronomic traits from Agropyron cristatum chromosome 1P. PLoS ONE 12:0175265. https://doi.org/10.1371/journal.pone.0175265
Qi L, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res 15(1):3–19. https://doi.org/10.1007/s10577-006-1108-8
Qi K, Han H, Zhang J, Zhou S, Li X, Yang X, Liu W, Lu Y, Li L (2021) Development and characterization of novel Triticum aestivum-Agropyron cristatum 6P Robertsonian translocation lines. Mol Breed 41(10):59. https://doi.org/10.1007/s11032-021-01251-y
Rabanus-Wallace MT, Hackauf B, Mascher M, Lux T, Stein N (2021) Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential. Nat Genet 5:564–573. https://doi.org/10.1038/s41588-021-00807-0
Rahmatov M, Rouse MN, Nirmala J, Danilova T, Friebe B, Steffenson BJ et al (2016) A new 2DS·2RL Robertsonian translocation transfers stem rust resistance gene Sr59 into wheat. Theor Appl Genet 129:1383–1392. https://doi.org/10.1007/s00122-016-2710-6
Robertson W (2005) Chromosome studies. I. Taxonomic relationships shown in the chromosomes of Tettegidae and Acrididiae : V-shaped chromsomes and their signivicance in Acrididae, Locustidae, and Grillidae: chromosomes and variations. J Morphol 27:179–331. https://doi.org/10.1002/jmor.1050270202
Ru Z, Feng S, Li G (2015) High-yield potential and effective ways of wheat in yellow & huai river valley facultative winter wheat region. Sci Agr 48:3388–3393. https://doi.org/10.3864/j.issn.0578-1752.2015.17.006
Sears ER (1952) Misdivision of univalents in common wheat. Chromosoma 4:535–550. https://doi.org/10.1007/BF00325789
Sun Y, Lyu M, Han H, Zhou S, Lu Y, Liu W, Yang X, Li X, Zhang J, Liu X, Li L (2021) Identification and fine mapping of alien fragments associated with enhanced grain weight from Agropyron cristatum chromosome 7P in common wheat backgrounds. Theor Appl Genet 134:3759–3772. https://doi.org/10.1007/s00122-021-03927-7
Tanaka H, Nabeuchi C, Kurogaki M, Garg M, Saito M, Ishikawa G, Nakamura T, Tsujimoto H (2017) A novel compensating wheat-Thinopyrum elongatum Robertsonian translocation line with a positive effect on flour quality. Breed Sci 67(5):509–517. https://doi.org/10.1270/jsbbs.17058
Tian J, Wang C, Xia J, Wu L, Xu G, Wu W, Li D, Qin W, Han X, Chen Q, Jin W, Tian F (2019) Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 365(6454):658–664. https://doi.org/10.1126/science.aax5482
Türkösi E, Darko E, Rakszegi M, Molnár I, Molnár-Láng M, Cseh A (2018) Development of a new 7BS.7HL winter wheat-winter barley Robertsonian translocation line conferring increased salt tolerance and (1,3;1,4)-β-D-glucan content. PLoS ONE 13:0206248. https://doi.org/10.1371/journal.pone.0206248
Villareal RL, RajaramMujeebkgazi SA, Toro E (1991) The effect of chromosome 1b/1r translocation on the yield potential of certain spring wheats (Triticum aestivum L.). Plant Breed 106:77–81. https://doi.org/10.1111/j.1439-0523.1991.tb00482.x
Wang X, Han B, Sun Y, Kang X, Zhang M, Han H, Zhou S, Liu W, Lu Y, Yang X, Li X, Zhang J, Liu X, Li L (2022) Introgression of chromosome 1P from Agropyron cristatum reduces leaf size and plant height to improve the plant architecture of common wheat. Theor Appl Genet 135:1951–1963. https://doi.org/10.1007/s00122-022-04086-z
Wickham H (2016) ggplot2-Elegant Graphics for Data Analysis, 2nd edn. Springer, New York
Zeller FJ, Koller OL (1981) Identification of a 4A/7R and a 7B/4R wheat-rye chromosome translocation. Theor Appl Genet 59:33–37. https://doi.org/10.1007/BF00275773
Zhang J, Liu W, Lu Y, Liu Q, Yang X, Li X, Li L (2017) A resource of large-scale molecular markers for monitoring Agropyron cristatum chromatin introgression in wheat background based on transcriptome sequences. Sci Rep 7:11942. https://doi.org/10.1038/s41598-017-12219-4
Zhang R, Hou F, Feng Y, Zhang W, Zhang M, Chen P (2015) Characterization of a Triticum aestivum-Dasypyrum villosum T2VS·2DL translocation line expressing a longer spike and more kernels traits. Theor Appl Genet 128:2415–2425. https://doi.org/10.1007/s00122-015-2596-8
Funding
This research was funded by the National Natural Science Foundation of China, grant number NSFC No. 31971879, and the Chinese Agriculture Research System, grant number CARS-03.
Author information
Authors and Affiliations
Contributions
Bohui Han and Xiao Wang have contributed equally to this work. LHL and JPZ conceived the research. BHH performed the research and wrote the paper. XW analyzed the data. YYS, XLK, MZ, and JWL collected the data, and HMH, SHZ, YQL, WHL, XMY, and XQL participated in the preparation of the reagents and materials in this study. All authors contributed to and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Ian D Godwin.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Han, B., Wang, X., Sun, Y. et al. Pre-breeding of spontaneous Robertsonian translocations for density planting architecture by transferring Agropyron cristatum chromosome 1P into wheat. Theor Appl Genet 137, 110 (2024). https://doi.org/10.1007/s00122-024-04614-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-024-04614-z