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A novel maize dwarf mutant generated by Ty1-copia LTR-retrotransposon insertion in Brachytic2 after spaceflight

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Abstract

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Retrotransposon insertion in Brachytic2 generated a new incomplete recessive dwarf allele after spaceflight can moderately reduce plant height in heterozygous and potentially improve maize yield.

Abstract

Plant height and ear height are two important agronomic traits in maize breeding. In this study, two dwarf mutants short internode length1 (sil1) and short internode length2 (sil2) were obtained from two of 398 spaceflighted seeds of inbred line 18-599. The decrease in longitudinal cell number and cell length led to the shortened internodes of sil1 and sil2. A Ty1-copia LTR-retrotransposon, termed ZmRE-1, inserted in the fifth exon of Brachytic2 (Br2) was identified in sil1 and sil2 at exactly the same site, which indicated the transposition of ZmRE-1 probably correlated with the spaceflight. This new dwarf mutant allele was named as br2-sil in this study. The insertion of ZmRE-1 not only led to the loss of normal transcript of Br2 allele, but also reduced the transcript expression of br2-sil allele. Chop-qPCR displayed that the promoter region DNA methylation level of br2-sil allele in sil1 was higher than that of Br2 allele in WT-sil1. We speculated that the increased methylation level might downregulate the br2-sil expression. There was no difference in the seed-setting rate between sil1 and WT-sil1. Meanwhile, br2-sil could reduce plant and ear height effectively in Br2/br2-sil genotype without negative effects on grain yield. Therefore, the application of br2-sil in breeding has the potential to improve the grain yield per unit area through increasing the planting density.

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References

  • Arena C, de Micco V, Macaeva E, Quintens R (2014) Space radiation effects on plant and mammalian cells. Acta Astronaut 104:419–431

    Article  CAS  Google Scholar 

  • Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7:75–84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brekke B, Edwards J, Knapp A (2011) Selection and adaptation to high plant density in the Iowa stiff stalk synthetic maize (Zea mays L.) population. Crop Sci 51:1965–1972

    Article  Google Scholar 

  • Cao Y, Jiang Y, Ding M, He S, Zhang H, Lin L, Rong J (2015) Molecular characterization of a transcriptionally active Ty1/copia-like retrotransposon in Gossypium. Plant Cell Rep 34(6):1037–1047

    Article  CAS  Google Scholar 

  • Chandler VL (2007) Paramutation: from maize to mice. Cell 128(4):641–645

    Article  CAS  Google Scholar 

  • Chen Y, Hou M, Liu L, Wu S, Shen Y, Ishiyama K, Kobayashi M, McCarty DR, Tan BC (2014) The maize DWARF1 encodes a gibberellin 3-oxidase and is dual-localized to the nucleus and cytosol. Plant Physiol 166:2028–2039

    Article  Google Scholar 

  • Cyranoski D (2001) Satellite will probe mutation seeds in space. Nature 410:857

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Fire A, Xu S, Montgomery M, Kostas S, Driver S, Mello C (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 39:806–811

    Article  Google Scholar 

  • Galindo-González L, Mhiri C, Deyholos MK, Grandbastien MA (2017) LTR-retrotransposons in plants: engines of evolution. Gene 626:14–25. https://doi.org/10.1016/j.gene.2017.04.051

    Article  CAS  PubMed  Google Scholar 

  • Grandbastien MA (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta 1849(4):403–416

    Article  CAS  Google Scholar 

  • Han FP, Liu ZL, Tan M, Hao S, Fedak G, Liu B (2004) Mobilized retrotransposon Tos17 of rice by alien DNA introgression transposes into genes and causes structural and methylation alterations of a flanking genomic region. Hereditas 141(3):243–251

    Article  CAS  Google Scholar 

  • Hollick JB (2017) Paramutation and related phenomena in diverse species. Nat Rev Genet 18(1):5–23. https://doi.org/10.1038/nrg.2016.115

    Article  CAS  PubMed  Google Scholar 

  • Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822

    Article  CAS  Google Scholar 

  • Knöller AS, Blakeslee JJ, Richards EL, Peer WA, Murphy AS (2010) Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. J Exp Bot 61:3689–3696

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Li Y, Liu M, Cheng Z, Sun Y (2007) Space environment induced mutations prefer to occur at polymorphic sites of rice genomes. Adv Space Res 40(4):523–527. https://doi.org/10.1016/j.asr.2007.04.100

    Article  CAS  Google Scholar 

  • Li H, Yang Q, Fan N, Zhang M, Zhai H, Ni Z, Zhang Y (2017) Quantitative trait locus analysis of heterosis for plant height and ear height in an elite maize hybrid zhengdan 958 by design III. BMC Genet 18:36. https://doi.org/10.1186/s12863-017-0503-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu L, Van Zanten L, Shu QY, Matuszynski M (2004a) Officially released mutant varieties in China. Mutat Breed Rev 14:1–62

    Google Scholar 

  • Liu Z, Han PF, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak G, Hao S, Liu B (2004b) Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. Theor Appl Genet 109:200–209

    Article  CAS  Google Scholar 

  • Livak KJ, Schmlaiittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CT) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Long L, Ou X, Liu J, Lin X, Sheng L, Liu B (2009) The spaceflight environment can induce transpositional activation of multiple endogenous transposable elements in a genotype-dependent manner in rice. J Plant Physiol 166(18):2035–2045. https://doi.org/10.1016/j.jplph.2009.06.007

    Article  CAS  PubMed  Google Scholar 

  • Mansfield BD, Mumm RH (2014) Survey of plant density tolerance in US. Maize Germplasm Crop Sci 54:157–173

    Article  Google Scholar 

  • Multani DS, Briggs SP, Chamberlin Ma, Blakeslee JJ, Murphy AS, Johal GS (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302:81–84

    Article  CAS  Google Scholar 

  • Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalconesynthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289

    Article  CAS  Google Scholar 

  • Nechitailo GS, Jinying L, Huai X, Yi P, Chongqin T, Min L (2005) Influence of long term exposure to space flight on tomato seeds. Adv Space Res 36(7):1329–1333. https://doi.org/10.1016/j.asr.2005.06.043

    Article  CAS  Google Scholar 

  • Peng JR, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  CAS  Google Scholar 

  • Pilu R (2015) Paramutation phenomena in plants. Semin Cell Dev Biol 44:2–10. https://doi.org/10.1016/j.semcdb.2015.08.015

    Article  CAS  PubMed  Google Scholar 

  • Ramallo E, Kalendar R, Schulman AH, Martínez-Izquierdo JA (2008) Reme1, a Copia retrotransposon in melon, is transcriptionally induced by UV light. Plant Mol Biol 66(1–2):137–150

    Article  CAS  Google Scholar 

  • Robbins ML, Sekhon RS, Meeley R, Chopra S (2008) A Mutator transposon insertion is associated with ectopic expression of a tandemly repeated multicopy Myb gene pericarp color1 of maize. Genetics 178(4):1859–1874. https://doi.org/10.1534/genetics.107.082503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353

    Article  CAS  Google Scholar 

  • Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) A mutant gibberellin-synthesis gene in rice. Nature 416(6882):701–702

    Article  CAS  Google Scholar 

  • Sher A, Khan A, Ashraf U, Liu HH, Li JC (2018) Characterization of the effect of increased plant density on canopy morphology and stalk lodging risk. Front Plant Sci 9:1047. https://doi.org/10.3389/fpls.2018.01047

    Article  PubMed  PubMed Central  Google Scholar 

  • Stam M (2009) Paramutation: a heritable change in gene expression by allelic interactions in trans. Mol Plant 2(4):578–588. https://doi.org/10.1093/mp/ssp020

    Article  CAS  PubMed  Google Scholar 

  • Stam M, Belele C, Dorweiler JE, Chandler VL (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16:1906–1918

    Article  CAS  Google Scholar 

  • Teng F, Zhai L, Liu R, Bai W, Wang L, Huo D, Tao Y, Zheng Y, Zhang Z (2012) ZmGA3ox2, a candidate gene for a major QTL, qPH3.1, for plant height in maize. Plant J 73:405–416

    Article  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  Google Scholar 

  • Wang Y, Deng D, Ding H, Xu X, Zhang R, Wang S, Bian Y, Yin Z, Chen Y (2013) Gibberellin biosynthetic deficiency is responsible for maize dominant Dwarf11 (D11) mutant phenotype: physiological and transcriptomic evidence. PLoS One 8(6):e66466. https://doi.org/10.1371/journal.pone.0066466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei L, Zhang X, Zhang Z, Liu H, Lin Z (2018) A new allele of the Brachytic2 gene in maize can efficiently modify plant architecture. Heredity (Edinb) 121(1):75–86

    Article  CAS  Google Scholar 

  • Winkler R, Helentjaris T (1995) The maize Dwarf3 gene encodes a cytochrome P450-mediated early step in gibberellin biosynthesis. Plant Cell 7:1307–1317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xing A, Gao Y, Ye L, Zhang W, Cai L, Ching A, Llaca V, Johnson B, Liu L, Yang X, Kang D, Yan J, Li J (2015) A rare SNP mutation in Brachytic2 moderately reduces plant height and increases yield potential in maize. J Exp Bot 66(13):3791–3802

    Article  CAS  Google Scholar 

  • Xue W, Xing Y, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    Article  CAS  Google Scholar 

  • Ya HY, Gu YH, Jiao Z, Wang WD, Qin GY, Huo YP (2007) Low-Energy Ion Beam Promotes the Transcription and Transposition of the Copia-retrotransposons in Wheat (Triticum aestivum L). J Plant Physiol Mol Biol 33(6):507–516

    CAS  Google Scholar 

  • Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH, Zhang YS, Yu SB, Xing YZ, Zhang QF (2011) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant 4:319–330

    Article  CAS  Google Scholar 

  • Yu X, Wu H, Wei LJ, Cheng ZL, Xin P, Huang C, Zhang K, Sun Y (2007) Characteristics of phenotype and genetic mutations in rice after spaceflight. Adv Space Res 40(4):528–534

    Article  CAS  Google Scholar 

  • Zhang CB, Wu ZD, Xu DP, Liu HY, Rong TZ, Cao MJ (2013) Combining ability analysis for SP4 lines of maize from space flight. Hereditas 35(7):903–912

    Article  Google Scholar 

  • Zhang H, Tang K, Wang B, Duan CG, Lang Z, Zhu JK (2014) Protocol: a beginner’s guide to the analysis of RNA-directed DNA methylation in plants. Plant Methods 10:18. https://doi.org/10.1186/1746-4811-10-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao HJ, Cui HR, Xu XH, Tan YY, Fu JJ, Liu GZ, Poirier Y, Shu QY (2013) Characterization of OsMIK in a rice mutant with reduced phytate content reveals an insertion of a rearranged retrotransposon. Theor Appl Genet 126(12):3009–3020. https://doi.org/10.1007/s00122-013-2189-3

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by The National Key Research and Development Program of China (No. 2016YFD0102104) and Platform for Mutation Breeding by Radiation in Sichuan (No. 2016NZ0106).

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  1. Chuan Li and Jin Tang contributed equally to this work.

Authors and Affiliations

  1. Maize Research Institute, Sichuan Agricultural University, No. 211 Huimin Road, Wenjiang District, Chengdu, 611130, China

    Chuan Li, Jin Tang, Zhaoyong Hu, Jingwen Wang, Tao Yu, Hongyang Yi & Moju Cao

  2. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, No. 211 Huimin Road, Wenjiang District, Chengdu, 611130, China

    Moju Cao

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  1. Chuan Li
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Contributions

CL and MC conceived and designed research. CL, JT, ZH and JW conducted experiments. CL and TY analyzed data. CL, HY and MC wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Moju Cao.

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Li, C., Tang, J., Hu, Z. et al. A novel maize dwarf mutant generated by Ty1-copia LTR-retrotransposon insertion in Brachytic2 after spaceflight. Plant Cell Rep 39, 393–408 (2020). https://doi.org/10.1007/s00299-019-02498-8

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