Cytogenetic analysis and molecular marker development for a novel wheat-Thinopyrum ponticum substitution line with leaf rust resistance

doi:10.11983/CBB25014

Abstract

Abstract: Abstract: The genetic diversity of common wheat (Triticum aestivum L.) has decreased sharply due to the artificial domestication and modern breeding operations, making it more vulnerable to the threats from pests and diseases. Introducing resistance genes from wild relatives into wheat through wide hybridization can broaden the genetic base of wheat and provide new sources for breeding disease-resistant varieties. As one of the most widely used relatives in the genetic improvement of wheat, decaploid Thinopyrum ponticum (Podp.) Barkworth and D. R. Dewey shows excellent resistance to multiple diseases including wheat rust. By wild hybridization and chromosome engineering, we created a wheat-Th. ponticum germplasm material WTS135, which showed immunity to the leaf rust pathogen Puccinia triticina Eriks. (Pt) race THTT. Pedigree analysis showed that this resistance originated from the exogenous chromosome of Th. ponticum. Sequential genomic in situ hybridization (GISH)-fluorescence in situ hybridization analysis revealed that the wheat chromosomes 7D were replaced by the Th. ponticum-derived chromosomes. Liquid chip showed that the alien chromosomes belonged to the homoeologous group 7, and the density and abundance of the signals in the peri-centromeric region along them were significantly lower, which was consistent with the GISH results. Therefore, it is indicated that WTS135 is a 7St (7D) disomic substitution line. After detected by the molecular markers related to known Lr genes on wheat 7D chromosome, it is presumed that WTS135 could carry a novel resistance gene that is not identical to genes Lr19 and Lr29. By specific-locus amplified fragment sequencing technology, ten primers specific to Th. ponticum were developed to rapidly trace the exogenous chromatin in WTS135. Phenotypic investigation showed that the yield of WTS135 was not significantly different from that of the recurrent parent Jimai 22, suggesting that this line can be useful for improving disease resistance in wheat.

Key words: Key words：wheat, Thinopyrum ponticum, leaf rust, wide hybridization, substitution line, in situ hybridization, molecular markers

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References

[1]Abhishek D.Tripathi, Richa Mishra, Kamlesh K. Maurya, Ram B. Singh, Douglas W. Wilson(2019).Chapter 1-Estimates for World Population and Global Food Availability for Global Health.New York: Academic Press, :3-24. [2]Deng PC, Du X, Wang YZ, Yang XY, Cheng XF, Huang CX, Li TT, Li TD, Chen CH, Zhao JX, Wang CY, Liu XL, Tian ZR, Ji WQ(2024).GenoBaits?WheatplusEE: a targeted capture sequencing panel for quick and accurate identification of wheat-Thinopyrum derivatives.Theoretical And Applied Genetics, 137:36-36. [3]Duan ZY, Xu XY, Li X, Li ZF, Ma J, Yao ZJ(2021).Leaf rust resistance gene analysis of 12 wheat cultivars in main producing areas.Crops, 37:20-27. [4]Friebe B, Jiang J, Gill BS, Dyck PL(1993).Radiation-induced nonhomoeologous wheat-Agropyron intermedium chromosomal translocations conferring resistance to leaf rust.Theoretical and Applied Genetics, 86:141-149. [5]Friebe B, Jiang J, Raupp W, McIntosh R, Gill B(1996).Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status.Euphytica, 91:59-87. [6]Fu SL, Lv ZL, Qi B, Guo X, Li J, Liu B, Han FP(2012).Molecular cytogenetic characterization of wheat-Thinopyrum elongatum addition,substitution and translocation lines with a novel source of resistance to wheat Fusarium Head Blight.Journal of Genetics and Genomics, 39:103-110. [7]Gupta SK, Charpe A, Prabhu KV, Haque QM(2006).Identification and validation of molecular markers linked to the leaf rust resistance gene Lr19 in wheat.Theoretical And Applied Genetics, 113:1027-1036. [8]Han F, Lamb JC, Birchler JA(2006).High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize.Proceedings of the National Academy of Sciences of the United States of America, 103:3238-3243. [9]He ZL, Zhang HK, Gao SH, Lercher MJ, Chen WH, Hu S(2016).Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees.Nucleic Acids Research, 44:236-241. [10]Huang XY, Zhu MQ, Zhuang LF, Zhang SY, Wang JJ, Chen XJ, Wang DR, Chen JY, Bao YG, Guo J, Zhang JL, Feng YG, Chu CG, Du P, Qi ZJ, Wang HG, Chen PD(2018).Structural chromosome rearrangements and polymorphisms identified in Chinese wheat cultivars by high-resolution multiplex oligonucleotide FISH.Theoretical And Applied Genetics, 131:1967-1986. [11]Ibba MI, Gupta OP, Govindan V, Johnson AAT, Brinch-Pedersen H, Nikolic M, Taleon V(2022).Editorial: Wheat biofortification to alleviate global malnutrition.Frontiers in Nutrition, 16:1001443-1001443. [12]Jiang J, Friebe B, Gill BS(1994).Chromosome painting of amigo wheat.Theoretical and Applied Genetics, 89:811-813. [13]Knott DR(1968).Translocations involving Triticum chromosomes and Agropyron chromosomes carrying rust resistance.Canadian Journal of Genetics and Cytology, 10:695-696. [14]Knott DR, Sharma D(1966).The transfer of leaf-rust resistance from Agropyron to Triticum by irradiation.Canadian Journal of Genetics and Cytology, 8:137-143. [15]Li J, Guan H, Wang Y, Dong C, Trethowan R, McIntosh RA, Zhang P(2024).Cytological and molecular characterization of wheat lines carrying leaf rust and stem rust resistance genes Lr24 and Sr24.Scientific Reports, 14:12816-12816. [16]Li MZ, Wang YZ, Liu XI, Li XF, Wang HG, Bao YQ(2021).Molecular Cytogenetic Identification of a novel wheat-Thinopyrum ponticum 1Js (1B) substitution line resistant to powdery mildew and leaf rust.Frontiers In Plant Science, 12:727734-727734. [17]Li ZS, Li B, Tong YP(2008).The contribution of distant hybridization with decaploid Agropyron elongatum to wheat improvement in China.Journal of Genetics and Genomics, 35:451-456. [18]Lin GF, Chen H, Tian B, Sehgal SK, Singh L, Xie JZ, Rawat N, Juliana P, Singh N, Shrestha S, Wilson DL, Shult H, Lee H, Schoen AW, Tiwari VK, Singh RP, Guttieri MJ, Trick HN, Poland J, Bowden RL, Bai GH, Gill B, Liu SZ(2022).Cloning of the broadly effective wheat leaf rust resistance gene Lr42 transferred from Aegilops tauschii.Nature Communications, 13:3044-3044. [19]Ling HQ, Ma B, Shi X, Liu H, Dong L, Sun H, Cao Y, Gao Q, Zheng S, Li Y, Yu Y, Du H, Qi M, Li Y, Lu H, Yu H, Cui Y, Wang N, Chen C, Wu H, Zhao Y, Zhang J, Li Y, Zhou W, Zhang B, Hu W, van Eijk MJT, Tang J, Witsenboer HMA, Zhao S, Li Z, Zhang A, Wang D, Liang C(2018).Genome sequence of the progenitor of wheat A subgenome Triticum urartu.Nature, 557:424-428. [20]Mago R, Zhang P, Xia XD, Zhang JP, Hoxha S, Lagudah E, Graner A, Dundas I(2019).Transfer of stem rust resistance gene SrB from Thinopyrum ponticum into wheat and development of a closely linked PCR-based marker.Theoretical And Applied Genetics, 132:371-382. [21]Mapuranga J, Chang J, Zhao J, Liang M, Li R, Wu Y, Zhang N, Zhang L, Yang W(2023).The underexplored mechanisms of wheat resistance to leaf rust.Plants (Basel), 12:3996-3996. [22]Niu Z, Klindworth DL, Yu G, L Friesen T, Chao S, Jin Y, Cai X, Ohm JB, Rasmussen JB, Xu SS(2014).Development and characterization of wheat lines carrying stem rust resistance gene Sr43 derived from Thinopyrum ponticum.Theoretical And Applied Genetics, 127:969-980. [23]Peto FH(1936).Hybridization of Triticum and Agropyron:II.cytology of the male parents and F1 generation. Canadian Respiratory Journal, 14:203-214. [24]Pirseyedi SM, Somo M, Poudel RS, Cai X, McCallum B, Saville B, Fetch T, Chao S, Marais F(2015).Characterization of recombinants of the Aegilops peregrina-derived Lr59 translocation of common wheat.Theoretical and Applied Genetics, 128:2403-2414. [25]Prasad P, Savadi S, Bhardwaj SC, Gupta PK(2020).The progress of leaf rust research in wheat.Fungal Biology, 124:537-550. [26]Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G(2012).Achieving yield gains in wheat.Plant Cell Environment, 35:1799-1823. [27]Roelfs AP, Singh RP, Saari EE(1992).Rust diseases of wheat: concepts and methods of disease management.Mexico: CIMMYT, :7-14. [28]Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW(1984).Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance,chromosomal location,and population dynamics.Proceedings of the National Academy of Sciences of the United States of America, 81:8014-8018. [29]Sears ER(1973).Agropyron-wheat transfers induced by homoeologous pairing.Columbia: University of Missouri, :191-199. [30]Sears ER(1977).Analysis of wheat-Agropyron recombinant chromosomes.Madrid: Eucarpia, :63-72. [31]Singh A, Pallavi JK, Gupta P, Prabhu KV(2012).Identification of microsatellite markers linked to leaf rust resistance gene Lr25 in wheat.Journal of Applied Genetics, 53:19-25. [32]Singh RP(2016).Disease impact on wheat yield potential and prospects of genetic control.Annual Review of Phytopathology, 54:303-322. [33]Smith EL, Schlehuber AM, Young HC, Edwards LH(1968).Registration of agent wheat1 (reg.no. 471).Crop Science, 8:511-512. [34]Tar M, Purnhauser L, Csosz L, Mesterházy, Gyulai G(2002).Identification of molecular markers for an efficient leaf rust resistance gene (Lr29) in wheat.Acta Biologica Szegediensis, 46:133-134. [35]Tsitsin NV(1965).Remote hybridisation as a method of creating new species and varieties of plants.Euphytica, 14:326-330. [36]Wang K, Li MY, Hakonarson H(2010).ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data.Nucleic Acids Research, 38:164-164. [37]Wang SW, Wang CY, Feng XB, Zhao JX, Deng PC, Wang YJ, Zhang H, Liu XL, Li TD, Chen CH, Wang BT, Ji WQ(2022).Molecular cytogenetics and development of St-chromosome-specific molecular markers of novel stripe rust resistant wheat-Thinopyrum intermedium and wheat-Thinopyrum ponticum substitution lines.BMC Plant Biology, 22:111-111. [38]Wang YZ, Cao Q, Zhang JI, Wang SW, Chen CH, Wang CY, Zhang H, Wang YI, Ji WQ(2020).Cytogenetic analysis and molecular marker development for a new wheat-Thinopyrum ponticum 1Js (1D) disomic substitution line with resistance to stripe rust and powdery mildew.Frontiers In Plant Science, 11:1282-1282. [39]Xu SS, Lyu ZF, Zhang N, Li MZ, Wei XY, Gao YH, Cheng XX, Ge WY, Li XF, Bao YG, Yang ZJ, Ma X, Wang HW, Kong LR(2023).Genetic mapping of the wheat leaf rust resistance gene Lr19 and development of translocation lines to break its linkage with yellow pigment.Theoretical And Applied Genetics, 136:200-200. [40]Yang GT, Deng PC, Ji WQ, Fu SL, Li HW, Li B, Li ZS, Zheng Q(2023).Physical mapping of a new powdery mildew resistance locus from Thinopyrum ponticum chromosome 4AgS.Frontiers in Plant Science, 14:1131205-1131205. [41]Zhang JL, Jie YZ, Yan LJ, Wang MM, Dong YL, Pang YF, Ren CC, Song J, Chen XD, Li XJ, Zhang PP, Yang DY, Zhang Y, Qi ZJ, Ru ZG(2024).Development and identification of a novel wheat-Thinopyrum ponticum disomic substitution line 5Ag (5D) with new genes conferring resistance to powdery mildew and leaf rust.BMC Plant Biology, 24:718-718. [42]Zhang L, Shi CC, Li LR, Li M, Meng QF, Yan HF, Liu DQ(2020).Race and Virulence Analysis of Puccinia triticina in China in 2014 and 2015.Plant Disease, 104:455-464. [43]Zhang W, Lukaszewski AJ, Kolmer J, Soria MA, Goyal S, Dubcovsky J(2005).Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum.Theoretical and Applied Genetics, 111:573-582. [44]Zhang XY, Dong YS, Wang RR(1996).Characterization of genomes and chromosomes in partial amphiploids of the hybrid Triticum aestivum × Thinopyrum ponticum by in situ hybridization,isozyme analysis,and RAPD.Genome, 39:1062-1071. [45]Zhao GY, Zou C, Li K, Wang K, Li TB, Gao LF, Zhang XX, Wang HJ, Yang ZJ, Liu X, Jiang WK, Mao L, Kong XY, Jiao YN, Jia JZ(2017).The Aegilops tauschii genome reveals multiple impacts of transposons.Nature Plants, 3:946-955. [46]Zhu C, Wang YZ, Chen CH, Wang CY, Zhang AC, Peng NN, Wang YJ, Zhang H, Liu XL, Ji WQ(2017).Molecular cytogenetic identification of a wheat-Thinopyrum ponticum substitution line with stripe rust resistance.Genome, 60:860-867.