Ancestral genome reconstruction and the evolution of chromosomal rearrangements in Triticeae

Xueqing Yan; Runxian Yu; Jinpeng Wang; Yuannian Jiao

doi:10.1016/j.jgg.2024.12.017

Volume 52 Issue 6

Jun. 2025

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Ancestral genome reconstruction and the evolution of chromosomal rearrangements in Triticeae

doi: 10.1016/j.jgg.2024.12.017

Xueqing Yan^a,b,c,
Runxian Yu^a,b,c,
Jinpeng Wang^a,b,c,d,
Yuannian Jiao^a,b,c

a. State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China;
b. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China;
c. University of Chinese Academy of Sciences, Beijing 100049, China;
d. School of Life Sciences and Center for Genomics and Computational Biology, North China University of Science and Technology, Tangshan, Hebei 063210, China

Funds:

This research was funded by CAS Youth Interdisciplinary Team (JCTD-2022-06) and the National Nature Science Foundation of China (31870209).

Received Date: 2024-08-15
Accepted Date: 2024-12-26
Rev Recd Date: 2024-12-25

Available Online: 2025-07-11

Publish Date: 2025-01-01

Abstract

Abstract

Chromosomal rearrangements (CRs) often cause phenotypic variations. Although several major rearrangements have been identified in Triticeae, a comprehensive study of the order, timing, and breakpoints of CRs has not been conducted. Here, we reconstruct high-quality ancestral genomes for the most recent common ancestor (MRCA) of the Triticeae, and the MRCA of the wheat lineage (Triticum and Aegilops). The protogenes of MRCA of the Triticeae and the wheat lineage are 22,894 and 29,060, respectively, which were arranged in their ancestral order. By partitioning modern Triticeae chromosomes into sets of syntenic regions and linking each to the corresponding protochromosomes, we revisit the rye chromosome structural evolution and propose alternative evolutionary routes. The previously identified 4L/5L reciprocal translocation in rye and Triticum urartu is found to have occurred independently and is unlikely to be the result of chromosomal introgression following distant hybridization. We also clarify that the 4AL/7BS translocation in tetraploid wheat was a bidirectional rather than unidirectional translocation event. Lastly, we identify several breakpoints in protochromosomes that independently reoccur following Triticeae evolution, representing potential CR hotspots. This study demonstrates that these reconstructed ancestral genomes can serve as special comparative references and facilitate a better understanding of the evolution of structural rearrangements in Triticeae.
- Chromosome rearrangement,
- Triticeae,
- Evolution,
- Ancestral genome reconstruction,
- Structure variations,
- Translocation

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References(81)

References

Al-Saghir, M.G., 2016. Taxonomy and phylogeny in Triticeae: a historical review and current status. Adv. Plants Agric. Res. 3, 139-143.

Alekseyev, M.A., Pevzner, P.A., 2009. Breakpoint graphs and ancestral genome reconstructions. Genome Res. 19, 943-957.

Alonge, M., Wang, X., Benoit, M., Soyk, S., Pereira, L., Zhang, L., Suresh, H., Ramakrishnan, S., Maumus, F., Ciren, D., et al., 2020. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell 182, 145-161.

Anderson, J.A., Ogihara, Y., Sorrells, M.E., Tanksley, S.D., 1992. Development of a chromosomal arm map for wheat based on RFLP markers. Theor. Appl. Genet. 83, 1035-1043.

Appels, R., Eversole, K., Feuillet, C., Keller, B., Rogers, J., Stein, N., Pozniak, C.J., Stein, N., Choulet, F., Distelfeld, A., et al. 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191.

Avdeyev, P., Jiang, S., Aganezov, S., Hu, F., Alekseyev, M.A., 2016. Reconstruction of Ancestral Genomes in Presence of Gene Gain and Loss. J. Comput. Biol. 23, 150-164.

Avni, R., Nave, M., Barad, O., Baruch, K., Twardziok, S.O., Gundlach, H., Hale, I., Mascher, M., Spannagl, M., Wiebe, K., et al., 2017. Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357, 93-97.

Ayala, F.J., Coluzzi, M., 2005. Chromosome speciation: humans, drosophila, and mosquitoes. Proc. Natl. Acad. Sci. U. S. A. 102, 6535-6542.

Cer, R.Z., Donohue, D.E., Mudunuri, U.S., Temiz, N.A., Loss, M.A., Starner, N.J., Halusa, G.N., Volfovsky, N., Yi, M., Luke, B.T., Bacolla, A., Collins, J.R., Stephens, R.M., 2013. Non-B DB v2.0: a database of predicted non-B DNA-forming motifs and its associated tools. Nucleic Acids Res. 41, D94-D100.

Chen, P.D., Qi, L.L., Zhou, B., Zhang, S.Z., Liu, D.J., 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, Y., Song, W., Xie, X., Wang, Z., Guan, P., Peng, H., Jiao, Y., Ni, Z., Sun, Q., Guo., W., 2020. A collinearity-incorporating homology inference strategy for connecting emerging assemblies in Triticeae tribe as a pilot practice in the plant pangenomic era. Mol. Plant 13, 1694–1708.

Daron, J., Glover, N., Pingault, L., Theil, S., Jamilloux, V., Paux, E., Barbe, V., Mangenot, S., Alberti, A., Wincker, P., Quesneville, H., Feuillet, C., Choulet, F., 2014. Organization and evolution of transposable elements along the bread wheat chromosome 3B. Genome Biol. 15, 546.

Devos, K.M., Atkinson, M.D., Chinoy, C.N., Francis, H.A., Harcourt, R.L., Koebner, R.M.D., Liu, C.J., Masojc, P., Xie, D.X., Gale, M.D., 1993. Chromosomal rearrangements in the rye genome relative to that of wheat. Theor. Appl. Genet. 85, 673-680.

Devos, K.M., Dubcovsky, J., Dvorak, J., Chinoy, C.N., Gale, M.D., 1995. Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor. Appl. Genet. 91, 282-288.

Dvorak, J., Wang, L., Zhu, T., Jorgensen, C.M., Luo, M.C., Deal, K.R., Gu, Y.Q., Gill, B.S., Distelfeld, A., Devos, K.M., et al., 2018. Reassessment of the evolution of wheat chromosomes 4A, 5A, and 7B. Theor. Appl. Genet. 131, 2451-2462.

Edgar, R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.

Eilam, T., Anikster, Y., Millet, E., Manisterski, J., Sagi-Assif, O., Feldman, M., 2007. Genome size and genome evolution in diploid Triticeae species. Genome 50, 1029-1037.

Emms, D.M., Kelly, S., 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238.

Faria, R., Navarro, A., 2010. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25, 660-669.

Friebe, B., Jiang, J., Raupp, W.J., McIntosh, R.A., Gill, B.S., 1996. Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91, 59-87.

Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., et al., 2011. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186.

Guo, J., Cao, K., Deng, C., Li, Y., Zhu, G., Fang, W., Chen, C., Wang, X., Wu, J., Guan, L., et al., 2020. An integrated peach genome structural variation map uncovers genes associated with fruit traits. Genome Biol. 21, 258.

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512.

He, Z., Ji, R., Havlickova, L., Wang, L., Li, Y., Lee, H.T., Song, J., Koh, C., Yang, J., Zhang, M., et al., 2021. Genome structural evolution in Brassica crops. Nat. Plants 7, 757-765.

Hernandez, P., Martis, M., Dorado, G., Pfeifer, M., Galvez, S., Schaaf, S., Jouve, N., Simkova, H., Valarik, M., Dolezel, J., et al., 2012. Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J. 69, 377-386.

Jorgensen, C., Luo, M.C., Ramasamy, R., Dawson, M., Gill, B.S., Korol, A.B., Distelfeld, A., Dvorak, J., 2017. A high-density genetic map of wild emmer wheat from the karaca dag region provides new evidence on the structure and evolution of wheat chromosomes. Front. Plant Sci. 8, 1798.

Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.

Kim, W., Johnson, J.W., Baenziger, P.S., Lukaszewski, A.J., Gaines, C.S., 2004. Agronomic effect of wheat-rye translocation carrying rye chromatin (1R) from different sources. Crop Sci. 44, 1254-1258.

Kim, J., Farre, M., Auvil, L., Capitanu, B., Larkin, D.M., Ma, J., Lewin, H.A., 2017. Reconstruction and evolutionary history of eutherian chromosomes. Proc. Natl. Acad. Sci. U. S. A. 114, E5379-E5388.

King, I.P., Purdie, K.A., Liu, C.J., Reader, S.M., Pittaway, T.S., Orford, S.E., Miller, T.E., 1994. Detection of interchromosomal translocations within the Triticeae by RFLP analysis. Genome 37, 882-887.

Li, B., Choulet, F., Heng, Y., Hao, W., Paux, E., Liu, Z., Yue, W., Jin, W., Feuillet, C., Zhang, X., 2013. Wheat centromeric retrotransposons: the new ones take a major role in centromeric structure. Plant J. 73, 952-965.

Li, W., Challa, G.S., 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.

Li, G., Wang, L., Yang, J., He, H., Jin, H., Li, X., Ren, T., Ren, Z., Li, F., Han, X., et al., 2021. A high-quality genome assembly highlights rye genomic characteristics and agronomically important genes. Nat. Genet. 53, 574-584.

Li, L.F., Zhang, Z.B., Wang, Z.H., Li, N., Sha, Y., Wang, X.F., Ding, N., Li, Y., Zhao, J., Wu, Y., et al., 2022. Genome sequences of five Sitopsis species of Aegilops and the origin of polyploid wheat B subgenome. Mol. Plant. 15, 488-503.

Ling, H.Q., Ma, B., Shi, X., Liu, H., Dong, L., Sun, H., Cao, Y., Gao, Q., Zheng, S., Li, Y., et al., 2018. Genome sequence of the progenitor of wheat A subgenome Triticum urartu. Nature 557, 424-428.

Liu, C.J., Atkinson, M.D., Chinoy, C.N., Devos, K.M., Gale, M.D., 1992. Nonhomoeologous translocations between group 4, 5 and 7 chromosomes within wheat and rye. Theor. Appl. Genet. 83, 305-312.

Liu, Y., Du, H., Li, P., Shen, Y., Peng, H., Liu, S., Zhou, G.A., Zhang, H., Liu, Z., Shi, M., et al., 2020. Pan-genome of wild and cultivated soybeans. Cell 182, 162-176.

Love A., 1984. Conspectus of the Triticeae. Feddes Repertorium 95, 425-521.

LU, B.R., ELLSTRAND, N., 2014. World food security and the tribe Triticeae (Poaceae): Genetic resources of cultivated, wild, and weedy taxa for crop improvement. J. Syst. Evol. 52, 661-666.

Luo, M.C., Gu, Y.Q., Puiu, D., Wang, H., Twardziok, S.O., Deal, K.R., Huo, N., Zhu, T., Wang, L., Wang, Y., et al., 2017. Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551, 498-502.

Ma, J., Stiller, J., Berkman, P.J., Wei, Y., Rogers, J., Feuillet, C., Dolezel, J., Mayer, K.F., Eversole, K., Zheng, Y.L., et al., 2013. Sequence-based analysis of translocations and inversions in bread wheat (Triticum aestivum L.). PLoS One 8, e79329.

Ma, J., Stiller, J., Wei, Y., Zheng, Y.L., Devos, K.M., Dolezel, J., Liu, C., 2014. Extensive pericentric rearrangements in the bread wheat (Triticum aestivum L.) genotype "Chinese Spring" revealed from chromosome shotgun sequence data. Genome Biol. Evol. 6, 3039-3048.

Maccaferri, M., Harris, N.S., Twardziok, S.O., Pasam, R.K., Gundlach, H., Spannagl, M., Ormanbekova, D., Lux, T., Prade, V.M., Milner, S.G., et al., 2019. Durum wheat genome highlights past domestication signatures and future improvement targets. Nat. Genet. 51, 885-895.

Martis, M.M., Zhou, R., Haseneyer, G., Schmutzer, T., Vrana, J., Kubalakova, M., Konig, S., Kugler, K.G., Scholz, U., Hackauf, B., et al., 2013. Reticulate evolution of the rye genome. Plant Cell 25, 3685-3698.

Mascher, M., Gundlach, H., Himmelbach, A., Beier, S., Twardziok, S.O., Wicker, T., Radchuk, V., Dockter, C., Hedley, P.E., Russell, J., et al., 2017. A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427-433.

Mascher, M., Wicker, T., Jenkins, J., Plott, C., Lux, T., Koh, C.S., Ens, J., Gundlach, H., Boston, L.B., Tulpova, Z., et al., 2021. Long-read sequence assembly: a technical evaluation in barley. Plant Cell 33, 1888-1906.

Miftahudin, Ross, K., Ma, X.F., Mahmoud, A.A., Layton, J., Milla, M.A., Chikmawati, T., Ramalingam, J., Feril, O., Pathan, M.S., et al., 2004. Analysis of expressed sequence tag loci on wheat chromosome group 4. Genetics 168, 651-663.

Monat, C., Padmarasu, S., Lux, T., Wicker, T., Gundlach, H., Himmelbach, A., Ens, J., Li, C., Muehlbauer, G.J., Schulman, A.H., et al., 2019. TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools. Genome Biol. 20, 284.

Murat, F., Pont, C., Salse, J., 2014. Paleogenomics in Triticeae for translational research. Curr. Plant Biol. 1, 34-39.

Murat, F., Armero, A., Pont, C., Klopp, C., Salse, J., 2017. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat. Genet. 49, 490-496.

Naranjo, T., Roca, A., Goicoechea, P.G., Giraldez, R.A.J.G., 1987. Arm homoeology of wheat and rye chromosomes. Genome 29, 873-882.

Navratilova, P., Toegelova, H., Tulpova, Z., Kuo, Y.T., Stein, N., Dolezel, J., Houben, A., Simkova, H., Mascher, M., 2022. Prospects of telomere-to-telomere assembly in barley: Analysis of sequence gaps in the MorexV3 reference genome. Plant Biotechnol. J. 20, 1373-1386.

Nelson, J.C., Sorrells, M.E., Van Deynze, A.E., Lu, Y.H., Atkinson, M., Bernard, M., Leroy, P., Faris, J.D., Anderson, J.A., 1995. Molecular mapping of wheat: major genes and rearrangements in homoeologous groups 4, 5, and 7. Genetics 141, 721-731.

Okonechnikov, K., Golosova, O., Fursov, M., UGENE team, 2012. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28, 1166-1167.

Perumal, S., Koh, C.S., Jin, L., Buchwaldt, M., Higgins, E.E., Zheng, C., Sankoff, D., Robinson, S.J., Kagale, S., Navabi, Z.K., et al., 2020. A high-contiguity Brassica nigra genome localizes active centromeres and defines the ancestral brassica genome. Nat. Plants 6, 929-941.

Rabanus-Wallace, M.T., Hackauf, B., Mascher, M., Lux, T., Wicker, T., Gundlach, H., Baez, M., Houben, A., Mayer, K.F.X., Guo, L., et al., 2021. Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential. Nat. Genet. 53, 564-573.

Raymond, O., Gouzy, J., Just, J., Badouin, H., Verdenaud, M., Lemainque, A., Vergne, P., Moja, S., Choisne, N., Pont, C., et al., 2018. The Rosa genome provides new insights into the domestication of modern roses. Nat. Genet. 50, 772-777.

Rieseberg, L.H., Livingstone, K., 2003. Chromosomal speciation in primates. Science 300, 267-268.

Ruban, A.S., Badaeva, E.D., 2018. Evolution of the S-genomes in Triticum-Aegilops alliance: Evidences from chromosome analysis. Front. Plant Sci. 9, 1756.

Salse, J., 2012. In silico archeogenomics unveils modern plant genome organisation, regulation and evolution. Curr. Opin. Plant Biol. 15, 122-130.

Sela, I., Ashkenazy, H., Katoh, K., Pupko, T., 2015. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 43, W7-W14.

Sharma, D., Knott, D.R., 1966. The transfer of leaf-rust resistance from Agropyron to Triticum by irradiation. Can. J. Genet. Cytol. 8,137-143.

Soltis, P.S., Marchant, D.B., Van de Peer, Y., Soltis, D.E., 2015. Polyploidy and genome evolution in plants. Curr. Opin. Genet. Dev. 35, 119-125.

Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.

Suyama, M., Torrents, D., Bork, P., 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609-W612.

Van de Peer, Y., Mizrachi, E., Marchal, K., 2017. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424.

Walkowiak, S., Gao, L., Monat, C., Haberer, G., Kassa, M.T., Brinton, J., Ramirez-Gonzalez, R.H., Kolodziej, M.C., Delorean, E., Thambugala, D., et al., 2020. Multiple wheat genomes reveal global variation in modern breeding. Nature 588, 277-283.

Wang, R.R.C., Lu, B., 2014. Biosystematics and evolutionary relationships of perennial Triticeae species revealed by genomic analyses. J. Syst. Evol. 52, 697-705.

Wang, Y., Tang, H., Debarry, J.D., Tan, X., Li, J., Wang, X., Lee, T.H., Jin, H., Marler, B., Guo, H., et al., 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49.

Wang, X., Wang, J., Jin, D., Guo, H., Lee, T.H., Liu, T., Paterson Andrew, H., 2015. Genome alignment spanning major poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events. Mol. Plant. 8, 885-898.

Wang, J., Sun, P., Li, Y., Liu, Y., Yu, J., Ma, X., Sun, S., Yang, N., Xia, R., Lei, T., et al., 2017. Hierarchically aligning 10 legume genomes establishes a family-level genomics platform. Plant Physiol. 174, 284-300.

Wang, H., Sun, S., Ge, W., Zhao, L., Hou, B., Wang, K., Lyu, Z., Chen, L., Xu, S., Guo, J., et al., 2020. Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368, eaba5435.

Wang, X., Hu, Y., He, W., Yu, K., Zhang, C., Li, Y., Yang, W., Sun, J., Li, X., Zheng, F., Zhou, S., Kong, L., Ling, H., Zhao, S., Liu, D., Zhang, A., 2022. Whole-genome resequencing of the wheat A subgenome progenitor Triticum urartu provides insights into its demographic history and geographic adaptation. Plant Commun. 3, 100345.

Wendel, J.F., Jackson, S.A., Meyers, B.C., Wing, R.A., 2016. Evolution of plant genome architecture. Genome Biol. 17, 37.

Wu, S., Shamimuzzaman, M., Sun, H., Salse, J., Sui, X., Wilder, A., Wu, Z., Levi, A., Xu, Y., Ling, K.S., et al., 2017. The bottle gourd genome provides insights into Cucurbitaceae evolution and facilitates mapping of a Papaya ring-spot virus resistance locus. Plant J. 92, 963-975.

Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.

Yang, Y., Cui, L., Lu, Z., Li, G., Yang, Z., Zhao, G., Kong, C., Li, D., Chen, Y., Xie, Z., Chen, Z., Zhang, L., Xia, C., Liu, X., Jia, J., Kong, X., 2023. Genome sequencing of Sitopsis species provides insights into their contribution to the B subgenome of bread wheat. Plant Commun. 4, 100567.

Zhao, C., Cui, F., Wang, X., Shan, S., Li, X., Bao, Y., Wang, H., 2012. Effects of 1BL/1RS translocation in wheat on agronomic performance and quality characteristics. Field Crop. Res. 127, 79-84.

Zhao, J., Xie, Y., Kong, C., Ku, Z., Jia, H., Ma, Z., Zhang, Y., Cui, D., Ru, Z., Wang, Y., Appels, R., Jia, J., Zhang, X., 2023. Centromere repositioning and shifts in wheat evolution. Plant Commun. 4,00556.

Zhao, G., Zou, C., Li, K., Wang, K., Li, T., Gao, L., Zhang, X., Wang, H., Yang, Z., Liu, X., et al., 2017. The Aegilops tauschii genome reveals multiple impacts of transposons. Nat. Plants 3, 946-955.

Zhou, Y., Bai, S., Li, H., Sun, G., Zhang, D., Ma, F., Zhao, X., Nie, F., Li, J., Chen, L., et al., 2021. Introgressing the Aegilops tauschii genome into wheat as a basis for cereal improvement. Nat. Plants 7, 774-786.

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