Skip to main content
SpringerLink
Log in

Loss of chromatin remodeler DDM1 causes segregation distortion in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

In ddm1 mutants, the DNA methylation is primarily affected in the heterochromatic region of the chromosomes, which is associated with the segregation distortion of SNPs in the F2 progenies.

Abstract

Segregation distortion (SD) is common in most genetic mapping experiments and a valuable resource to determine how gene loci induce deviation. Meiotic DNA crossing over and SD are under the control of several types of epigenetic modifications. DNA methylation is an important regulatory epigenetic modification that is inherited across generations. In the present study, we investigated the relationship between SD and DNA methylation. The ecotypes Col-0/C24 and chromatin remodeler mutants ddm1-10/Col and ddm1-15/C24 were reciprocally crossed to obtain F2 generations. A total of 300 plants for each reciprocally crossed plant in the F2 generations were subjected to next-generation sequencing to detect the single-nucleotide polymorphisms (SNPs) as DNA markers. All SNPs were analyzed using the Chi-square test method to determine their segregation ratio in F2 generations. Through the segregation ratio, whole-genome SNPs were classified into 16 classes. In class 10, the SNPs in the reciprocal crosses of wild type showed the expected Mendelian ratio of 1:2:1, while those in the reciprocal crosses of ddm1 mutants showed distortion. In contrast, all SNPs in class 16 displayed a normal 1:2:1 ratio, and class 1 showed SD, regardless of wild type or mutants, as assessed using CAPS (cleaved amplified polymorphic sequences) marker analysis to confirm the next-generation sequencing. In ddm1 mutants, the DNA methylation is highly reduced throughout the whole genome and more significantly in the heterochromatic regions of chromosomes. Our results showed that the ddm1 mutants exhibit low levels of DNA methylation, which facilitates the SD of SNPs primarily located in the heterochromatic region of chromosomes by reducing the heterozygous ratio. The present study will provide a strong base for future research focusing on the impact of DNA methylation on trait segregation and plant evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The DNA methylation data that support the findings of this study are available in NCBI Gene Expression Omnibus (GEO) www.ncbi.nlm.nih.gov/geo (accession no. GSE72993). Genomic sequencing data in NCBI under accession no. GSE74551 and GSE72993.

Abbreviations

CAPS:

Cleaved amplified polymorphic sequences

CO:

Crossing over

DMR:

Differentially methylated region

SNP:

Single-nucleotide polymorphism

SD:

Segregation distortion

References

  • Acquaviva L, Székvölgyi L, Dichtl B, Dichtl BS, Saint André CdLR, Nicolas A, Géli V (2013) The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339:215–218

    Article  PubMed  CAS  Google Scholar 

  • Adamski T, Krystkowiak K, Kuczyńska A, Mikołajczak K, Ogrodowicz P, Ponitka A, Ślusarkiewicz-Jarzina A (2014) Segregation distortion in homozygous lines obtained via anther culture and maize doubled haploid methods in comparison to single seed descent in wheat (Triticum aestivum L.). Electron J Biotechnol 17(1):6–13

    Article  CAS  Google Scholar 

  • Baumbach J, Rogers JP, Slattery RA, Narayanan NN, Xu M, Palmer RG, Sandhu D (2012) Segregation distortion in a region containing a male-sterility, female-sterility locus in soybean. Plant Sci 195:151–156

    Article  PubMed  CAS  Google Scholar 

  • Blackwell AR, Dluzewska J, Szymanska-Lejman M, Desjardins S, Tock AJ, Kbiri N, Henderson IR (2020) MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis. EMBO J 39(21):e104858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Charlesworth B (1988) Driving genes and chromosomes. Nature 332(6163):394–395

    Article  PubMed  CAS  Google Scholar 

  • Choi K, Henderson IR (2015) Meiotic recombination hotspots—a comparative view. Plant J 83(1):52–61

    Article  PubMed  CAS  Google Scholar 

  • Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, Yelina NE, Hardcastle TJ, Ziolkowski PA, Copenhaver GP, Franklin FC, McVean G (2013) Arabidopsis meiotic crossover hot spots overlap with H2A. Z nucleosomes at gene promoters. Nat Genet 45(11):1327–1336

    Article  PubMed  CAS  Google Scholar 

  • Choi K, Zhao X, Tock AJ, Lambing C, Underwood CJ, Hardcastle TJ, Serra H, Kim J, Cho HS, Kim J, Ziolkowski PA, Yelina NE, Hwang I, Martienssen RA, Henderson IA (2018) Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Res 28:523–546

    Article  CAS  Google Scholar 

  • Colomé-Tatché M, Cortijo S, Wardenaar R et al (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci USA 109(40):16240–16245

    Article  PubMed  PubMed Central  Google Scholar 

  • Coulton A, Przewieslik-Allen AM, Burridge AJ, Shaw DS, Edwards KJ, Barker GL (2020) Segregation distortion: utilizing simulated genotyping data to evaluate statistical methods. PLoS ONE 15(2):e0228951

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dai B, Guo H, Huang C, Ahmed MM, Lin Z (2017) Identification and characterization of segregation distortion loci on cotton chromosome 18. Front Plant Sci 12(7):2037

    Google Scholar 

  • Fernandes JB, Wlodzimierz P, Henderson IR (2019) Meiotic recombination within plant centromeres. Curr Opin Plant Biol 48:26–35

    Article  PubMed  CAS  Google Scholar 

  • Fishman L, Aagaard J, Tuthill JC (2008) Toward the evolutionary genomics of gametophytic divergence: patterns of transmission ratio distortion in monkeyflower (Mimulus) hybrids reveal a complex genetic basis for conspecific pollen precedence. Evolution 62(12):2958–2970

    Article  PubMed  Google Scholar 

  • Fojtová M, Kovařík A, Matyášek R (2001) Cytosine methylation of plastid genome in higher plants. Fact or artefact? Plant Sci 160:585–593. https://doi.org/10.1016/S0168-9452(00)00411-8

    Article  PubMed  Google Scholar 

  • Gartner GAL, McCouch SR, Moncada MDP (2013) A genetic map of an interspecific diploid pseudo testcross population of coffee. Euphytica 192(2):305–323

    Article  CAS  Google Scholar 

  • Guo W, Cai C, Wang C, Han Z, Song X, Wang K, Niu X, Wang C, Lu K, Shi B, Zhang T (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in Gossypium. Genetics 176(1):527–541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He Y, Wang M, Dukowic-Schulze S, Zhou A, Tiang CL, Shilo S, Sidhu GK, Eichten S, Bradbury P, Springer NM, Buckler ES (2017) Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize. Proc Natl Acad Sci USA 114(46):12231–12236

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu G, Cui K, Northrup D, Liu C, Wang C, Tang Q, Ge K, Levens D, Crane-Robinson C, Zhao K (2013) H2A Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Sell 12(2):180–192

    Article  CAS  Google Scholar 

  • Iwasaki M (2015) Chromatin resetting mechanisms preventing transgenerational inheritance of epigenetic states. Front Plant Sci 6:380. https://doi.org/10.3389/fpls.2015.00380

    Article  PubMed  PubMed Central  Google Scholar 

  • Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112(6):308–315

    Article  PubMed  CAS  Google Scholar 

  • Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22(1):94–97

    Article  PubMed  CAS  Google Scholar 

  • Jeffreys AJ, Neumann R, Panayi M, Myers S, Donnelly P (2005) Human recombination hot spots hidden in regions of strong marker association. Nat Genet 37(6):601–606

    Article  PubMed  CAS  Google Scholar 

  • Kakutani T, Munakata K, Richards EJ, Hirochika H (1999) Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151(2):831–838

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kianian PMA, Wang M, Simons K et al (2018) High-resolution crossover mapping reveals similarities and differences of male and female recombination in maize. Nat Commun 9:2370. https://doi.org/10.1038/s41467-018-04562-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kitashiba H, Taguchi K, Kaneko I, Inaba K, Yokoi S, Takahata Y, Nishio T (2016) Identification of loci associated with embryo yield in microspore culture of Brassica rapa by segregation distortion analysis. Plant Cell Rep 35(10):2197–2204

    Article  PubMed  CAS  Google Scholar 

  • Lambing C, Franklin FCH, Wang CJR (2017) Understanding and manipulating meiotic recombination in plants. Plant Physiol 173(3):1530–1542

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larracuente AM, Presgraves DC (2012) The selfish segregation distorter gene complex of Drosophila melanogaster. Genetics 192(1):33–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lawrence EJ, Griffin CH, Henderson IR (2017) Modification of meiotic recombination by natural variation in plants. J Exp Bot 68(20):5471–5483

    Article  PubMed  CAS  Google Scholar 

  • Leppälä J, Bokma F, Savolainen O (2013) Investigating incipient speciation in Arabidopsis lyrata from patterns of transmission ratio distortion. Genetics 194(3):697–708

    Article  PubMed  PubMed Central  Google Scholar 

  • Li C, Bai G, Chao S, Wang Z (2015) A high-density SNP and SSR consensus map reveals segregation distortion regions in wheat. Biomed Res Int 2015:1–10. https://doi.org/10.1155/2015/830618

    Article  CAS  Google Scholar 

  • Li X, Singh J, Qin M, Li S, Zhang X, Zhang M, Khan A, Zhang S, Wu J (2019) Development of an integrated 200K SNP genotyping array and application for genetic mapping, genome assembly improvement and genome wide association studies in pear (Pyrus). Plant Biotechnol J 17(8):1582–1594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133(3):523–536

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu JJ, Zhao HY, Suo NN, Wang S, Shen B, Wang HZ, Liu JJ (2012) Genetic linkage maps of Dendrobium moniliforme and D. officinale based on EST-SSR, SRAP, ISSR and RAPD markers. Sci Hortic 137:1–10

    Article  CAS  Google Scholar 

  • Lyttle TW (1993) Cheaters sometimes prosper: distortion of mendelian segregation by meiotic drive. Trends Genet 9(6):205–210

    Article  PubMed  CAS  Google Scholar 

  • Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454(7203):479–485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mangelsdorf PC, Jones DF (1926) The expression of Mendelian factors in the gametophyte of maize. Genetics 11(5):423–455

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15(6):394–408

    Article  PubMed  CAS  Google Scholar 

  • Melamed-Bessudo C, Levy AA (2012) Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci USA 109(16):E981–E988

    Article  PubMed  PubMed Central  Google Scholar 

  • Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M (2015) The molecular biology of meiosis in plants. Annu Rev Plant Biol 66:297–327. https://doi.org/10.1146/annurev-arplant-050213-035923

    Article  PubMed  CAS  Google Scholar 

  • Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J, Reinders J, Paszkowski J (2012) Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci USA 109(15):5880–5885

    Article  PubMed  PubMed Central  Google Scholar 

  • Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411(6834):212–214

    Article  PubMed  CAS  Google Scholar 

  • Morgan TH (1911) Random segregation versus coupling in Mendelian inheritance. Science 34(873):384–384

    Article  PubMed  CAS  Google Scholar 

  • Orr HA, Irving S (2005) Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169(2):671–682

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, Zhu X, Neale MJ, Jasin M, Socci ND, Hochwagen A (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144(5):719–731

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plough LV, Hedgecock D (2011) Quantitative trait locus analysis of stage-specific inbreeding depression in the Pacific oyster Crassostrea gigas. Genetics 189(4):1473–1486

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodgers-Melnick E, Bradbury PJ, Elshire RJ, Glaubitz JC, Acharya CB, Mitchell SE, Li C, Li Y, Buckler ES (2015) Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc Natl Acad Sci USA 112:3823–3828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmid KJ, Sörensen TR, Stracke R, Törjék O, Altmann T, Mitchell-Olds T, Weisshaar B (2003) Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res 13:1250–1257

    Article  PubMed  PubMed Central  Google Scholar 

  • Shanmugavadivel PS, Mithra SA, Dokku P, Kumar KAR, Rao GJN, Singh VP, Singh AK, Singh NK, Mohapatra T (2013) Mapping quantitative trait loci (QTL) for grain size in rice using a RIL population from Basmati × indica cross showing high segregation distortion. Euphytica 194(3):401–416

    Article  CAS  Google Scholar 

  • Shi J, Wolf SE, Burke JM, Presting GG, Ross-Ibarra J, Dawe RK (2010) Widespread gene conversion in centromere cores. PLoS Biol 8(3):e1000327. https://doi.org/10.1371/journal.pbio.1000327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sommermeyer V, Benéut C, Chaplais E, Serrentino ME, Borde V (2013) Spp1, a member of the Set1 complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol Cell 49:43–54

    Article  PubMed  CAS  Google Scholar 

  • Takumi S, Motomura Y, Iehisa JCM, Kobayashi F (2013) Segregation distortion caused by weak hybrid necrosis in recombinant inbred lines of common wheat. Genetica 141:463–470

    Article  PubMed  Google Scholar 

  • Tan Y, Cahan P (2019) SingleCellNet: a computational tool to classify single cell RNA-Seq data across platforms and across species. Cell Syst 28(2):207–213

    Article  CAS  Google Scholar 

  • Tan F, Lu Y, Jiang W, Wu T, Zhang R, Zhao Y, Zhou DX (2018) DDM1 represses noncoding RNA expression and RNA-directed DNA methylation in heterochromatin. Plant Physiol 177(3):1187–1197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20(6):244–251

    Article  PubMed  CAS  Google Scholar 

  • Underwood CJ, Choi K, Lambing C, Zhao X, Serra H, Borges F, Simorowski J, Ernst E, Jacob Y, Henderson IR, Martienssen RA (2018) Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation. Genome Res 28(4):519–531. https://doi.org/10.1101/gr.227116.117

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xi Y, Li W (2009) BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinform 10:232

    Article  CAS  Google Scholar 

  • Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, Qiu S, Huang J, Jiang Y, Jiang L, Ding J (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337(6100):1336–1340

    Article  PubMed  CAS  Google Scholar 

  • Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B, Wijnker E, Miller N, Drouaud J, Grelon M, Copenhaver GP, Mezard C (2012) Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet 8:e1002844

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yelina NE, Lambing C, Hardcastle TJ, Zhao X, Santos B, Henderson IR (2015) DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev 29(20):2183–2202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zamariola L, Tiang CL, De Storme N, Pawlowski W, Geelen D (2014) Chromosome segregation in plant meiosis. Front Plant Sci 5:279

    Article  PubMed  PubMed Central  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153(1):193–205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Li XuT, Srivastava AK, Wang D, Zeng L, Yang L, He L, Zhang H, Zheng Z, Yang DL, Zhao C, Dong J, Gong Z, Liu R, Zhu JK (2016a) The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism. Cell Discov 2:16027. https://doi.org/10.1038/celldisc.2016.27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Q, Wang D, Lang Z, He L, Yang L, Zeng L, Li Y, Zhao C, Huang H, Zhang H, Zhang H, Zhu JK (2016b) Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation. Proc Natl Acad Sci USA 113(29):E4248–E4256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou W, Tang Z, Hou J, Hu N, Yin T (2015) Genetic map construction and detection of genetic loci underlying segregation distortion in an intraspecific cross of Populus deltoides. PLoS ONE 10(5):e0126077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank all the members of Qingzhu Zhang lab Northeast Forestry University Harbin, China, especially Jie Zou, Dr. Bowei Chen, Dr. Min Wang, Wei Zhou, Dr. Lishan Wang, and Dr. Wang Yu for useful discussion.

Funding

This work was supported by the National Natural Science Foundation of China (31871220); the National Nonprofit Institute Research Grant of the Chinese Academy of Forestry (CAFYBB2019ZY003); the Fundamental Research Funds for the Central Universities (2572017DA06 and 2572020DP01). CL receives BBSRC grant-aided support as part of the Institute Strategic Program Designing Future Wheat Grant (BB/P016855/1).

Author information

Author notes

  1. Shahid Ali and Tianxu Zhang contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Science, Northeast Forestry University, Harbin, 150040, China

    Shahid Ali, Wanpeng Wang, Peng Zhang, Linan Xie & Jiang Wang

  2. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China

    Tianxu Zhang & Qingzhu Zhang

  3. College of Life Sciences, Northeast Forestry University, Harbin, 150040, China

    Tianxu Zhang, Linan Xie, Jiang Wang & Qingzhu Zhang

  4. Plant Sciences Department, Rothamsted Research, Harpenden, AL5 2JQ, UK

    Christophe Lambing

  5. Department of Agronomy, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, 32611, USA

    Naeem Khan

Authors
  1. Shahid Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tianxu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christophe Lambing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wanpeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Linan Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Naeem Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qingzhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qingzhu Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Dorothea Bartels.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 4805 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ali, S., Zhang, T., Lambing, C. et al. Loss of chromatin remodeler DDM1 causes segregation distortion in Arabidopsis thaliana. Planta 254, 107 (2021). https://doi.org/10.1007/s00425-021-03763-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-021-03763-5

Keywords

Search

Navigation