Abstract
Key message
We developed an array of Zea–Tripsacum tri-hybrid allopolyploids with multiple ploidies. We unveiled that changes in genome dosage due to the chromosomes pyramiding and shuffling of three species effects karyotypic heterogeneity, reproductive diversity, and phenotypic variation in Zea–Tripsacum allopolyploids.
Abstract
Polyploidy, or whole genome duplication, has played a major role in evolution and speciation. The genomic consequences of polyploidy have been extensively studied in many plants; however, the extent of chromosomal variation, genome dosage, phenotypic diversity, and heterosis in allopolyploids derived from multiple species remains largely unknown. To address this question, we synthesized an allohexaploid involving Zea mays, Tripsacum dactyloides, and Z. perennis by chromosomal pyramiding. Subsequently, an allooctoploid and an allopentaploid were obtained by hybridization of the allohexaploid with Z. perennis. Moreover, we constructed three populations with different ploidy by chromosomal shuffling (allopentaploid × Z. perennis, allohexaploid × Z. perennis, and allooctoploid × Z. perennis). We have observed 3 types of sexual reproductive modes and 2 types of asexual reproduction modes in the tri-species hybrids, including 2n gamete fusion (2n + n), haploid gamete fusion (n + n), polyspermy fertilization (n + n + n) or 2n gamete fusion (n + 2n), haploid gametophyte apomixis, and asexual reproduction. The tri-hybrids library presents extremely rich karyotype heterogeneity. Chromosomal compensation appears to exist between maize and Z. perennis. A rise in the ploidy of the trihybrids was linked to a higher frequency of chromosomal translocation. Variation in the degree of phenotypic diversity observed in different segregating populations suggested that genome dosage effects phenotypic manifestation. These findings not only broaden our understanding of the mechanisms of polyploid formation and reproductive diversity but also provide a novel insight into genome pyramiding and shuffling driven genome dosage effects and phenotypic diversity.
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References
Antonarakis SE, Lyle R, Dermitzakis ET, Reymond A, Deutsch S (2004) Chromosome 21 and down syndrome: from genomics to pathophysiology. Nat Rev Genet 5:725–738. https://doi.org/10.1038/nrg1448
Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402. https://doi.org/10.1105/tpc.106.049338
Birchler JA, Veitia RA (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc Natl Acad Sci U S A 109:14746–14753. https://doi.org/10.1073/pnas.1207726109
Birchler JA, Yao H, Chudalayandi S, Vaiman D, Vaiman RA (2010) Heterosis. Plant Cell 22:2105–2112. https://doi.org/10.1105/tpc.110.076133
Blakeslee AF (1928) Genetics in Datura. Z Indukt Abstamm Vererbungsl 1(Suppl):117–130
Cao Y, Zhao K, Xu J, Wu L, Hao F, Sun M, Dong J, Chao G, Zhang H, Gong X, Chen Y, Chen C, Qian W, Pires JC, Edger PP, Xiong Z (2023) Genome balance and dosage effect drive allopolyploid formation in Brassica. Proc Natl Acad Sci U S A 120:e2217672120. https://doi.org/10.1073/pnas.2217672120
Chalhoub B, Denoeud F, Liu S et al (2014) Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953. https://doi.org/10.1126/science.1253435
Chase SS (1980) Studies of monoploid, diploid and tetraploids of maize in relation to heterosis and inbreeding depression. In: Proceedings of the argentine society of genetics.
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406. https://doi.org/10.1146/annurev.arplant.58.032806.103835
Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71. https://doi.org/10.1016/j.tplants.2009.12.003
Chen ZJ, Sreedasyam A, Ando A et al (2020) Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement. Nat Genet 52:525–533. https://doi.org/10.1038/s41588-020-0614-5
Chester M, Gallagher JP, Symonds VV, Cruz da Silva AV, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE (2012) Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci U S A 109:1176–1181. https://doi.org/10.1073/pnas.1112041109
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846. https://doi.org/10.1038/nrg1711
de Wet JMJ, Harlan JR (1974) Tripsacum-maize interaction: a novel cytogenetic system. Genetics 78:493–502. https://doi.org/10.1093/genetics/78.1.493
de Wet JMJ, Lambert RJ, Harlan JR, Naik SM (1970) Stable triploid hybrids among Zea-Tripsacum-Zea back-cross populations. Caryologia 23:183–187
Dewhurst SM, McGranahan N, Burrell RA, Rowan AJ, Grönroos E, Endesfelder D, Joshi T, Mouradov D, Gibbs P, Ward RL, Hawkins NJ, Szallasi Z, Sieber OM, Swanton C (2014) Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov 4:175–185. https://doi.org/10.1158/2159-8290.CD-13-0285
Doebley JF (1990) Molecular evidence and the evolution of maize. Econ Bot 44:6–27. https://doi.org/10.1007/BF02860472
Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Ann Rev Genet 42:443–461. https://doi.org/10.1146/annurev.genet.42.110807.091524
Feldman M, Levy AA (2012) Genome evolution due to allopolyploidization in wheat. Genetics 192:763–774. https://doi.org/10.1534/genetics.112.146316
Fort A, Ryder P, McKeown PC, Wijnen C, Aarts MG, Sulpice R, Spillane C (2016) Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New Phytol 209:590–599. https://doi.org/10.1111/nph.13650
Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417. https://doi.org/10.1105/tpc.107.054346
Galinat WC (1983) The origin of maize as shown by key morphological traits of its ancestor, teosinte. Maydica 28:121–138
Gault CM, Kremling KA, Buckler ES (2018) Tripsacum de novo transcriptome assemblies reveal parallel gene evolution with maize after ancient polyploidy. Plant Genome 11:180012. https://doi.org/10.3835/plantgenome2018.02.0012
Gou X, Bian Y, Zhang A, Zhang H, Wang B, Lv R, Li J, Zhu B, Gong L, Liu B (2018) Transgenerationally precipitated meiotic chromosome instability fuels rapid karyotypic evolution and phenotypic diversity in an artificially constructed allotetraploid wheat (AADD). Mol Biol Evol 35:1078–1091. https://doi.org/10.1093/molbev/msy009
Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966–971. https://doi.org/10.1111/j.1469-8137.2012.04365.x
Harlan JR, de Wet JMJ (1977) Pathways of genetic transfer from Tripsacum to Zea mays. Proc Natl Acad Sci U S A 74:3494–3497. https://doi.org/10.1073/pnas.74.8.3494
Hufford MB, Bilinski P, Pyhäjärvi T, Ross-Ibarra J (2012) Teosinte as a model system for population and ecological genomics. Trends Genet 28:606–615. https://doi.org/10.1016/j.tig.2012.08.004
Iqbal MZ, Cheng M, Su Y, Li Y, Jiang W, Li H, Zhao Y, Wen X, Zhang L, Ali A, Rong T, Tang Q (2019) Allopolyploidization facilitates gene flow and speciation among corn, Zea perennis and Tripsacum dactyloides. Planta 249:1949–1962. https://doi.org/10.1007/s00425-019-03136-z
Iqbal MZ, Wen X, Xu L, Zhao Y, Li J, Jiang W, Cheng M, Li H, Li Y, Li X, He R, He J, Su Y, Ali A, Peng Y, Rong T, Tang Q (2023) Multispecies polyploidization, chromosome shuffling, and genome extraction in Zea/Tripsacum hybrids. Genetics 223:iyad029. https://doi.org/10.1093/genetics/iyad029
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100. https://doi.org/10.1038/nature09916
Kato A, Birchler JA (2006) Induction of tetraploid derivatives of maize inbred lines by nitrous oxide gas treatment. J Hered 97:39–44. https://doi.org/10.1093/jhered/esj007
Kindiger B, Beckett JB (1992) Popcorn germplasm as a parental source for maize × Tripsacum dactyloides hybridization. Maydica 37:245–249
Kindiger B, Sokolov V, Dewald C (1996a) A comparison of apomictic reproduction in eastern gamagrass (Tripsacum dactyloides (L.) L.) and maize-Tripsacum hybrids. Genetica 97:103–110. https://doi.org/10.1007/BF00132586
Kindiger B, Sokolov V, Khatypova IV (1996b) Evaluation of apomictic reproduction in a set of 39 chromosome maize-Tripsacum backcross hybrids. Crop Sci 36:1108–1113. https://doi.org/10.2135/cropsci1996.0011183X003600050006x
Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–1228. https://doi.org/10.1093/genetics/150.3.1217
Lamb JC, Birchler JA (2006) Retroelement genome painting: cytological visualization of retroelement expansions in the genera Zea and Tripsacum. Genetics 173:1007–1021. https://doi.org/10.1534/genetics.105.053165
Landis JB, Soltis DE, Li Z, Marx HE, Barker MS, Tank DC, Soltis PS (2018) Impact of whole-genome duplication events on diversification rates in angiosperms. Am J Bot 105:348–363. https://doi.org/10.1002/ajb2.1060
Lee MS, Anderson EK, Stojšin D, McPherson MA, Baltazar B, Horak MJ, de la Fuente JM, Wu K, Crowley JH, Rayburn AL, Lee DK (2017) Assessment of the potential for gene flow from transgenic maize (Zea mays L.) to eastern gamagrass (Tripsacum dactyloides L.). Transgenic Res 26:501–514. https://doi.org/10.1007/s11248-017-0020-7
Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483. https://doi.org/10.1126/science.1153585
Levings CS, Dudley JW, Alexander DE (1967) Inbreeding and crossing in autotetraploid maize. Crop Sci 7:72–73. https://doi.org/10.2135/cropsci1967.0011183X000700010025x
Li H, Cheng M, Su Y, Li Z, Jiang W, Zhang H, Zheng M, Rong T, Zhou S, Wu Y, Cao M, Tang Q (2015) Chromosomal composition and forage production potential of Yuqilin 58. Acta Prataculturae Sinica 24:157–163. https://doi.org/10.11686/cyxb20150419
Li Z, McKibben MTW, Finch GS, Blischak PD, Sutherland BL, Barker MS (2021) Patterns and processes of diploidization in land plants. Annu Rev Plant Biol 72:387–410. https://doi.org/10.1146/annurev-arplant-050718-100344
Li Y, Yan X, Li X, Chen Y, Li W, Xu L, He J, Rong T, Tang Q (2022) Advances in research and utilization of maize wild relatives. Chin Sci Bull 67:4370–4387. https://doi.org/10.1360/TB-2022-0669
Lv R, Wang C, Wang R, Wang X, Zhao J, Wang B, Aslam T, Han F, Liu B (2022) Chromosomal instability and phenotypic variation in a specific lineage derived from a synthetic allotetraploid wheat. Front Plant Sci 13:981234. https://doi.org/10.3389/fpls.2022.981234
Mangelsdorf PC, Reeves RG (1931) Hybridization of maize, Tripsacum, and Euchlaena. J Hered 22:329–343. https://doi.org/10.1093/oxfordjournals.jhered.a103401
Mangelsdorf PC, Reeves RG (1935) A trigeneric hybrid of Zea Tripsacum and Euchlaena: all of the chromosomes of maize and its two nearest relatives combined in a single plant. J Hered 26:129–140. https://doi.org/10.1093/oxfordjournals.jhered.a104052
Mirzaghaderi G, Mason AS (2017) Revisiting pivotal-differential genome evolution in wheat. Trends Plant Sci 22:674–684. https://doi.org/10.1016/j.tplants.2017.06.003
Newell CA, de Wet JMJ (1973) A cytological survey of Zea–Tripsacum hybrids. Can J Genet Cytol 15:763–778. https://doi.org/10.1139/g73-090
Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331. https://doi.org/10.1038/nature07523
Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462. https://doi.org/10.1016/j.cell.2007.10.022
Ramachandran D, McKain MR, Kellogg EA, Hawkins JS (2020) Evolutionary dynamics of transposable elements following a shared polyploidization event in the Tribe Andropogoneae. G3 (Bethesda) 10:4387–4398. https://doi.org/10.1534/g3.120.401596
Ramírez-González RH, Borrill P, Lang D et al (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089. https://doi.org/10.1126/science.aar6089
Randolph LF (1942) The influence of heterozygosis on fertility and vigor in autotetraploid maize. Genetics 27:163
Riddle NC, Birchler JA (2008) Comparative analysis of inbred and hybrid maize at the diploid and tetraploid levels. Theor Appl Genet 116:563–576. https://doi.org/10.1007/s00122-007-0691-1
Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci U S A 108:4069–4074. https://doi.org/10.1073/pnas.1101368108
Shi X, Yang H, Chen C, Hou J, Hanson KM, Albert PS, Ji T, Cheng J, Birchler JA (2021) Genomic imbalance determines positive and negative modulation of gene expression in diploid maize. Plant Cell 33:917–939. https://doi.org/10.1093/plcell/koab030
Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588. https://doi.org/10.1146/annurev.arplant.043008.092039
Soltis PS, Soltis DE (2016) Ancient WGD events as drivers of key innovations in angiosperms. Curr Opin Plant Biol 30:159–165. https://doi.org/10.1016/j.pbi.2016.03.015
Van de Peer Y, Ashman TL, Soltis PS, Soltis DE (2021) Polyploidy: an evolutionary and ecological force in stressful times. Plant Cell 33:11–26. https://doi.org/10.1093/plcell/koaa015
Wang X, Wang H, Wang J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039. https://doi.org/10.1038/ng.919
Washburn JD, Birchler JA (2014) Polyploids as a “model system” for the study of heterosis. Plant Reprod 27:1–5. https://doi.org/10.1007/s00497-013-0237-4
Washburn JD, McElfresh MJ, Birchler JA (2019) Progressive heterosis in genetically defined tetraploid maize. J Genet Genom 46:389–396. https://doi.org/10.1016/j.jgg.2019.02.010
Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249. https://doi.org/10.1023/A:1006392424384
Xiong Z, Gaeta T, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci U S A 108:7908–7913. https://doi.org/10.1073/pnas.1014138108
Yan X, Cheng M, Li Y, Wu Z, Li Y, Li X, He R, Yang C, Zhao Y, Li H, Wen X, Zhang P, Sam E, Rong T, He J, Tang Q (2020) Tripsazea, a novel trihybrid of Zea mays, Tripsacum dactyloides, and Zea perennis. G3 (Bethesda) 10:839–848. https://doi.org/10.1534/g3.119.400942
Yan X, Li Y, Wu Z, Li Y, Wen X, Li X, He R, Yang C, Zhao Y, Cheng M, Zhang P, Sam EK, Rong T, He J, Tang Q (2020b) Analysis of the genitor origin of an intergeneric hybrid clone between Zea and Tripsacum for forage production by McGISH. Breed Sci 70:241–245. https://doi.org/10.1270/jsbbs.19107
Yang H, Shi X, Chen C, Hou J, Ji T, Cheng J, Birchler JA (2021) Predominantly inverse modulation of gene expression in genomically unbalanced disomic haploid maize. Plant Cell 33:901–916. https://doi.org/10.1093/plcell/koab029
Yao H, Kato A, Mooney B, Birchler JA (2011) Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol Biol 75:237–251. https://doi.org/10.1007/s11103-010-9722-4
Yao H, Dogra Gray A, Auger DL, Birchler JA (2013) Genomic dosage effects on heterosis in triploid maize. Proc Natl Acad Sci U S A 110:2665–2669. https://doi.org/10.1073/pnas.1221966110
Zhang H, Bian Y, Gou X, Dong Y, Rustgi S, Zhang B, Xu C, Li N, Qi B, Han F, von Wettstein D, Liu B (2013a) Intrinsic karyotype stability and gene copy number variations may have laid the foundation for tetraploid wheat formation. Proc Natl Acad Sci U S A 110:19466–19471. https://doi.org/10.1073/pnas.1319598110
Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F, Jiang J, von Wettstein D, Liu B (2013b) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proc Natl Acad Sci U S A 110:3447–3452. https://doi.org/10.1073/pnas.1300153110
Acknowledgements
The authors are deeply grateful for the availability of the maize-Tripsacum hybrid. The authors also thank James Schnable and two anonymous reviewers for criticism and suggestions.
Funding
This work was supported by the Department of Science and Technology of Sichuan Province (grant No.2022NSFSC0167), National Natural Science Foundation of China (Grant No. 32272035); the Forage Breeding Projects of Sichuan Province during the 14th 5-Year Plan Period (Grant No. 2021YFYZ0013-3); the Sichuan Corn Innovation Team of National Modern Agricultural Industry Technology System (Grant No. sccxtd-2020-02); the Sichuan Science and Technology Program (Grant No. MZGC20230107), Sichuan Science and Technology Innovation and Entrepreneurship Seedling Project (key project) (Grant No. 2023JDRC0117).
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QT, TR, and YL conceived the study. JH and XY supervised the study. YL, XY, ZW, QZ, MC, SD, YZ, HL, SY, YC, WL, LX, and CY performed the experiments YL, XY, XL, RH, and YZ analyzed the data YL, XY, MC, MZI, and QT prepared and revised the manuscript. All authors reviewed the manuscript.
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Li, Y., Yan, X., Cheng, M. et al. Genome dosage alteration caused by chromosome pyramiding and shuffling effects on karyotypic heterogeneity, reproductive diversity, and phenotypic variation in Zea–Tripsacum allopolyploids. Theor Appl Genet 137, 28 (2024). https://doi.org/10.1007/s00122-023-04540-6
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DOI: https://doi.org/10.1007/s00122-023-04540-6