Abstract
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High-resolution multiplex oligonucleotide FISH revealed the frequent occurrence of structural chromosomal rearrangements and polymorphisms in widely grown wheat cultivars and their founders.
Abstract
Over 2000 wheat cultivars including 19 founders were released and grown in China from 1949 to 2000. To understand the impact of breeding selection on chromosome structural variations, high-resolution karyotypes of Chinese Spring (CS) and 373 Chinese cultivars were developed and compared by FISH (fluorescence in situ hybridization) using an oligonucleotide multiplex probe based on repeat sequences. Among them, 148 (39.7%) accessions carried 14 structural rearrangements including three single translocations (designated as T), eight reciprocal translocations (RT), one pericentric inversion (perInv), and two combined variations having both the deletion and single translocations. Five rearrangements were traced to eight founders, including perInv 6B detected in 57 cultivars originating from Funo, Abbondanza, and Fan 6, T 1RS∙1BL in 47 cultivars derived from the Lovrin series, RT 4AS∙4AL-1DS/1DL∙1DS-4AL in 31 varieties from Mazhamai and Bima 4, RT 1RS∙7DL/7DS∙1BL in three cultivars was from Aimengniu, and RT 5BS∙5BL-5DL/5DS∙5DL-5BL was only detected in Youzimai. In addition to structural rearrangements, 167 polymorphic chromosome blocks (defined as unique signal patterns of oligonucleotide repeat probes distributed within chromosomes) were identified, and 59 were present in one or more founders. Some specific types were present at high frequencies indicating selective blocks in Chinese wheat varieties. All cultivars and CS were clustered into four groups and 15 subgroups at chromosome level. Common block patterns occurred in the same subgroup. Origin, geographic distribution, probable adaptation to specific environments, and potential use of these chromosomal rearrangements and blocks are discussed.
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References
Badaeva ED, Dedkova OS, Gay G, Pukhalskyi VA, Zelenin AV, Bernard S, Bernard M (2007) Chromosomal rearrangements in wheat: their types and distribution. Genome 50:907–926. https://doi.org/10.1139/G07-072
Bie T, Zhao R, Zhu S, Chen S, Cen B, Zhang B, Gao D, Jiang Z, Chen T, Wang L, Wu R, Wu R, He H (2015) Development and characterization of marker MBH1, simultaneously tagging genes Pm21, and PmV, conferring resistance to powdery mildew in wheat. Mol Breeding 35:189. https://doi.org/10.1007/s11032-015-0385-3
Cai X, Liu D (1989) Identification of a 1B/1R wheat-rye chromosome translocation. Theor Appl Genet 77:81–83. https://doi.org/10.1007/BF00292320
Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci USA 108:7727–7732. https://doi.org/10.1073/pnas.1016981108
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110:8057–8062. https://doi.org/10.1073/pnas.1217133110
Chan SWL (2010) Chromosome engineering: power tools for plant genetics. Trends Biotechnol 28:605–610. https://doi.org/10.1016/j.tibtech.2010.09.002
Doležel J, Číhalíková J, Lucretti S (1992) A high-yield procedure for isolation of metaphase chromosomes from root tips of Vicia faba L. Planta 188:93–98. https://doi.org/10.1007/BF00198944
Du P, Zhuang L, Wang Y, Yuan L, Wang Q, Wang D, Dawadondup Tan L, Shen J, Xu H, Zhao H, Chu C, Qi Z (2017) Development of oligonucleotides and multiplex probes for quick and accurate identification of wheat and Thinopyrum bessarabicum chromosomes. Genome 60:93–103. https://doi.org/10.1139/gen-2016-0095
Feldman M, Levy AA (2012) Genome evolution due to allopolyploidization in wheat. Genetics 192:763–774. https://doi.org/10.1534/genetics.112.146316
Friebe B, Gill BS (1994) C-band polymorphism and structural rearrangements detected in common wheat (Triticum aestivum). Euphytica 78:1–5. https://doi.org/10.1007/bf00021392
Han J, Zhang LS, Li JT, Shi LJ, Xie CJ, You MS, Yang ZM, Liu GT, Sun QX, Liu ZY (2009) Molecular dissection of core parental cross “Triumph/Yanda 1817” and its derivatives in wheat breeding program. Acta Agron Sin 35:1395–1404. https://doi.org/10.3724/SP.J.1006.2009.01395 (in Chinese with English abstract)
Hao C, Wang L, Zhang X, You G, Dong Y, Jia J, Liu X, Shang X, Liu S, Cao Y (2006) Genetic diversity in Chinese modern wheat varieties revealed by microsatellite markers. Sci Sin Vitae 49:218–226. https://doi.org/10.1007/s11427-006-0218-z (in Chinese with English abstract)
Hao C, Wang Y, Chao S, Li T, Liu H, Wang L, Zhang X (2017) The iSelect 9 K SNP analysis revealed polyploidization induced revolutionary changes and intense human selection causing strong haplotype blocks in wheat. Sci Reports 7:41247. https://doi.org/10.1038/srep41247
Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, Wilkinson PA, Salazar C, Davidson C, Clark R, Quail MA, Beasley H, Glithero R, Lloyd C, Sims S, Jones MC, Rogers J, Jiggins CD, ffrench-Constant RH (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203–206. https://doi.org/10.1038/nature10341
Kato A (1999) Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 74:160–166. https://doi.org/10.3109/10520299909047968
Li H, Chen X, Xin Z, Ma Y, Xu H (2000) Development and identification of wheat Haynaldia villosa 6DL/6VS translocation lines with powdery mildew resistance. Sci Agric Sin 1:10–16. https://doi.org/10.3321/j.issn:0578-1752.1999.05.002 (in Chinese with English abstract)
Li W, Challa GS, Zhu H, Wei W (2016) Recurrence of chromosome rearrangements and reuse of DNA breakpoints in the evolution of the Triticeae genomes. G3 6:3837–3847. https://doi.org/10.1534/g3.116.035089
Liu K, Muse SV (2005) PowerMaker: an integrated analysis environment for genetic maker analysis. Bioinformatics 21:2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Liu XL, Si QL, Li QQ, Wang CY, Wang YJ, Zhang H, Ji WQ (2012) SSR Analysis of genetic diversity and temporal trends of the core wheat (Triticum aestivum L.) parent Funo and its derivative varieties (lines). J Agric Biotechnol 20:983–995. https://doi.org/10.3969/j.issn.1674-7968.2012.09.002 (in Chinese with English abstract)
Mukai Y, Endo T, Gill B (1991) Physical mapping of the 18S. 26S rRNA multigene family in common wheat: identification of a new locus. Chromosoma 100:71–78. https://doi.org/10.1007/bf00418239
Nei MF, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153–170. https://doi.org/10.1007/bf02300753
Qi ZJ, Chen PD, Liu DJ, Li QQ (2004) A new secondary reciprocal translocation discovered in Chinese wheat. Euphytica 137:333–338. https://doi.org/10.1023/B:EUPH.0000040454.11647.59
Schneider A, Linc G, Molnár-Láng M (2003) Fluorescence in situ hybridization polymorphism using two repetitive DNA clones in different cultivars of wheat. Plant Breed 122:396–400. https://doi.org/10.1046/j.1439-0523.2003.00891.x
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731. https://doi.org/10.1093/molbev/msr121
Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422. https://doi.org/10.1007/s00122-002-1031-0
Wang D, Du P, Pei Z, Zhuang L, Qi Z (2017) Development and application of high resolution karyotypes of Chinese Spring aneuploids. Acta Agron Sin 43:1575–1587. https://doi.org/10.3724/SP.J.1006.2017.01575 (in Chinese with English abstract)
Xiang JS, Yang XM, Li XQ, Liu WH, Gao AN, Li LH, Ma XG (2013) The analysis of HMW-GS evolution in Mentana and its derivations. J Plant Genet Resour 14:1053–1058. https://doi.org/10.13430/j.cnki.jpgr.2013.06.013 (in Chinese with English abstract)
Xu X, Li XJ, Li XQ, Yang XM, Liu WH, Gao AN, Li LH (2010) Inheritance of 1BL/1RS of founder parent Lovrin 10 in its progeny. J Triticeae Crops 30:221–226. https://doi.org/10.7606/j.issn.1009-1041.2010.02.007 (in Chinese with English abstract)
Yu HX, Xiao J, Tian JC (2012) Genetic dissection of milestone parent Aimengniu and its derivatives. Sci Agric Sin 45:199–207. https://doi.org/10.3864/j.issn.0578-1752.2012.02.001 (in Chinese with English abstract)
Yuan YY, Wang QZ, Cui F, Zhang JT, Du B, Wang HG (2010) Specific loci in genome of wheat milestone parent Bima 4 and their transmission in derivatives. Acta Agron Sin 36:9–16. https://doi.org/10.3724/SP.J.1006.2010.00009 (in Chinese with English abstract)
Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F, Jiang J, Wettstein D, Liu B (2013) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proc Natl Acad Sci USA 110:3447–3452. https://doi.org/10.1073/pnas.1300153110
Zhang X, Zhang BQ, Jiang W, Lv GF, Zhang XX, Li M, Gao DR (2015) Molecular detection for quality traits-related genes in Yangmai series wheat cultivars. Sci Agric Sin 48:3779–3793. https://doi.org/10.3864/j.issn.0578-1752.2015.19.001 (in Chinese with English abstract)
Zhong S, Yao J (1994) Cytogenetic studies on a reciprocal translocation between chromosomes 1B and 4A in common wheat. Jiangsu J Agric Sci 10:1–5 (in Chinese with English abstract)
Zhou Y, He Z, Zhang G, Xia L, Chen X, Gao Y, Jing Z, Yu G (2004) Utilization of 1BL/1RS translocation in wheat breeding in China. Acta Agron Sin 30:531–535. https://doi.org/10.3321/j.issn:0496-3490.2004.06.003 (in Chinese with English abstract)
Zhuang Q (2003) Chinese wheat improvement and pedigree analysis. China Agriculture Press, Beijing, pp 1–419
Acknowledgements
This project was supported by National Natural Science Foundation of China (31671681; 31370385) and the Fundamental Research Funds for the Central Universities (Y0201700147). Our thanks go to Prof. Zhengqiang Ma, Nanjing Agricultural University, Nanjing, Prof. Lihui Li, Chinese Academy of Agriculture Sciences, Beijing, and Prof. Jishan Niu, Henan Agricultural University, Zhengzhou, Henan, for review and suggestions on improving the manuscript, Prof. Xueyong Zhang, Chinese Academy of Agriculture Sciences, Beijing, for donating seeds of Aegilops speltoides and Triticum urartu, and Prof. Hisashi Tsujimoto, Arid Land Research Center, Tottori University, Japan, for donating seeds of Aegilops squarrosa. Thanks to Robert McIntosh, University of Sydney, Australia, for kind review, many suggestions, and editing. Xiejun Sun and Heng Nie kindly helped in preparing the manuscript. Our thanks also go to the editor and anonymous reviewers for critical comments and suggestions for improving the manuscript.
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Fig. S1
Pericentric inversion in chromosome 6B. CS and inverted ideotypes are shown left and right, respectively. Red signals show oligonucleotides pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 modified with TAMRA, green show pSc119.2-1 and (GAA)10 modified with FAM (TIFF 1277 kb)
Fig. S2
Oligonucleotide multiplex painted karyotypes of cultivars with the pericentric inversion of 6B. Colors, as in Fig. S1 (TIFF 72694 kb)
Fig. S3
Oligonucleotide multiplex painted karyotypes of cultivars containing T 1RS•1BL. Colors, as in Fig. S1 (TIFF 57405 kb)
Fig. S4
Identification of T 1RS•1BL in Lovrin 10 (17Z064) and RT 1RS•7DL / 7DS•1BL in Aimengniu (17Z225). a, b, and c II, chromosomes after GISH/FISH using multiplex probes containing Secale cereale genomic DNA labeled with fluorescein-12-dUTP (green), TAMRA-modified oligonucleotide probes pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 (red), and FAM-modified pSc119.2-1 and (GAA)10 (green). c I, Chromosomes after FISH using the oligonucleotide multiplex probe containing FAM-modified pSc119.2-1 and (GAA)10 (green), TAMRA-modified pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 (red). a, Lovrin 10 (17Z064). b, Aimengniu (17Z225). c, Karyotypes of Lovrin 10 and Aimengniu (TIFF 22357 kb)
Fig. S5
Oligonucleotide multiplex painted karyotypes of cultivars containing RT 4AS•4AL-1DS/1DL•1DS-4AL from Mazhamai (17Z377), a Chinese landrace. Red signals show oligonucleotides pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 modified with TAMRA, green shows pSc119.2-1 and (GAA)10 modified with FAM (TIFF 33455 kb)
Fig. S6
Karyotypes of cultivars with 11 structural rearrangements detected in chromosomes of widely grown Chinese wheat cultivars, except T 1RS•1BL, RT 1RS•7DL / 7DS•1BL and perInv 6B. Red signals show oligonucleoties pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 modified with TAMRA, green shows pSc119.2-1 and (GAA)10 modified with FAM. *, translocation or deletion chromosome (TIFF 34253 kb)
Fig. S7
Identification of RT 4AS•4AL-1BL / 1BS•1BL-4AL in accession 17Z283 (Xiangnong 2170-7-27). a, Chromosome FISH using the oligonucleotide multiplex probe containing pSc119.2-1 (green), (GAA)10 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4(red); b, chromosome FISH using multiplex probes containing the SS genome labeled with fluorescein-12-dUTP (green), (GAA)10 (red), and pSc119.2-1 (red) after FISH. c, Karyotype of CS and 17Z283, I: probes as shown in a, II: probes as shown in b. * translocation chromosome(TIFF 16114 kb)
Fig. S8
Identification of T 1BL•1RS and RT 2AL•2AS-5BL / 5BS•5BL-2AS in accession 17Z340 (Xiangnong 153-27). a, Chromosome FISH of CS using multiplex probe containing the SS genome (green), (GAA)10 (red) and pSc119.2-1 (red). b, Chromosome FISH of accession 17Z340 using multiplex probe containing the SS genome (green), (GAA)10 (red), and pSc119.2-1 (red). c, Karyotype of CS and 17Z340 (A and B genomes), I : probes using multiplex probe containing (GAA)10 (green), pSc119.2-1 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red). II: CS, probes using multiplex probe containing (GAA)10 (green), pSc119.2-1 (green); 17Z340, probes as shown in b; III: CS, probes as shown in a. * translocation chromosome (TIFF 26068 kb)
Fig. S9
Identification of 1B deletion and T 1BS-3DS•3DL in accession 17Z172 (Shannongfu 63). a and b, Sequential FISH with 45S rDNA plasmid clones labeled with digoxigenin-11-dUTP (red), and oligonucleotides pSc119.2-1 (green), (GAA)10 (green) (a), and pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red) (b) on chromosomes of accession 17Z172. c, Multiplex FISH-based karyotype of 17Z172, i: probes using multiplex probes containing (GAA)10 (green), pSc119.2-1 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red); ii: sequential FISH karyotype using 45S rDNA plasmid clones labeled with digoxigenin-11-dUTP (red), and oligonucleotides pSc119.2-1 (green), (GAA)10 (green) as shown in a; iii: probes using oligonucleotides pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red) as shown in b. d, Chromosome FISH of 17Z172 using the multiplex oligonucleotides probe containing pSc119.2-1 (green), (GAA)10 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red). e and f, Chromosome FISH of 17Z172 (e) and CS (f) using multiplex probe containing 45S rDNA plasmid clones labeled with digoxigenin-11-dUTP (red), pSc119.2-1(green), and (GAA)10 (green). g, Chromosomes 1A, 1B, 6B, 3D, 5D, and 7D of CS and 17Z172. I: multiplex probe using (GAA)10 (green), pSc119.2-1 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red). II, Multiplex probe using 45S rDNA plasmid clones labeled with digoxigenin-11-dUTP (red), and oligonucleotides (GAA)10 (green), pSc119.2-1 (green). III, From different cells of 17Z172, probes as shown in II. * translocation or deletion chromosome (TIFF 30058 kb)
Fig. S10
Identification of T 6VS•6AL in YM18 (Yangmai 18) and T 6VS•6DL in YM22 (Yangmai 22). a, b, and c II, Chromosome FISH using multiplex probes containing the Haynaldia villosa genome labeled with fluorescein-12-dUTP (green), pSc119.2-1 (green), (GAA)10 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4 (red). cI, Chromosome FISH using the oligonucleotide multiplex probe containing pSc119.2-1 (green), (GAA)10 (green), pAs1-1 (red), pAs1-3 (red), pAs1-4 (red), pAs1-6 (red), AFA-3 (red), and AFA-4(red). a, Yangmai 18. b, Yangmai 22. c, Karyotype of Yangmai 18 and Yangmai 22. * translocation chromosome (TIFF 17637 kb)
Fig. S11
Lovrin 10 (accession 17Z064) and part derivatives. Red signals show oligonucleoties pAs1-1, pAs1-3, pAs1-4, pAs1-6, AFA-3, and AFA-4 modified with TAMRA, green show pSc119.2-1 and (GAA)10 modified with FAM (TIFF 13829 kb)
Fig. S12
Funo (accession 17Z379) and derivatives (left: A and right: B). Colors, as in Fig. S1 (TIFF 6798 kb)
Fig. S13
Xiaoyan 6 (accession 17Z298) and derivatives. Colors, as in Fig. S1 (TIFF 27191 kb)
Fig. S14
Yanda 1817 (accession 17Z141) and derivatives. Colors, as in Fig. S1 (TIFF 28654 kb)
Fig. S15
Nanda 2419 (accession 17Z343) and derivatives. Colors, as in Fig. S1 (TIFF 117414 kb)
Fig. S16
Bima selections and their derivatives. Colors, as in Fig. S1 (TIFF 112782 kb)
Fig. S17
Other accessions. Colors, as in Fig. S1 (TIFF 44883 kb)
Fig. S18
Cluster analysis of 373 Chinese wheat cultivars and Chinese Spring based on structural rearrangements and polymorphic blocks (DOCX 660 kb)
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Huang, X., Zhu, M., Zhuang, L. et al. Structural chromosome rearrangements and polymorphisms identified in Chinese wheat cultivars by high-resolution multiplex oligonucleotide FISH. Theor Appl Genet 131, 1967–1986 (2018). https://doi.org/10.1007/s00122-018-3126-2
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DOI: https://doi.org/10.1007/s00122-018-3126-2