Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm

. 2021 Feb ; 17 (2) : e1009370. [epub] 20210211

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33571184
Odkazy

PubMed 33571184
PubMed Central PMC7904229
DOI 10.1371/journal.pgen.1009370
PII: PGENETICS-D-20-01346
Knihovny.cz E-zdroje

Hybridization of closely related plant species is frequently connected to endosperm arrest and seed failure, for reasons that remain to be identified. In this study, we investigated the molecular events accompanying seed failure in hybrids of the closely related species pair Capsella rubella and C. grandiflora. Mapping of QTL for the underlying cause of hybrid incompatibility in Capsella identified three QTL that were close to pericentromeric regions. We investigated whether there are specific changes in heterochromatin associated with interspecific hybridizations and found a strong reduction of chromatin condensation in the endosperm, connected with a strong loss of CHG and CHH methylation and random loss of a single chromosome. Consistent with reduced DNA methylation in the hybrid endosperm, we found a disproportionate deregulation of genes located close to pericentromeric regions, suggesting that reduced DNA methylation allows access of transcription factors to targets located in heterochromatic regions. Since the identified QTL were also associated with pericentromeric regions, we propose that relaxation of heterochromatin in response to interspecies hybridization exposes and activates loci leading to hybrid seed failure.

Zobrazit více v PubMed

Li J, Berger F. Endosperm: Food for humankind and fodder for scientific discoveries. New Phytol. 2012;195: 290–305. 10.1111/j.1469-8137.2012.04182.x PubMed DOI

Leblanc O, Pointe C, Hernandez M. Cell cycle progression during endosperm development in Zea mays depends on parental dosage effects. Plant J. 2002;32: 1057–1066. 10.1046/j.1365-313x.2002.01491.x PubMed DOI

Lin BY. Ploidy barrier to endosperm development in maize. Genetics. 1984;107: 103–15. PubMed PMC

Costa LM, Gutièrrez-Marcos JF, Dickinson HG. More than a yolk: The short life and complex times of the plant endosperm. Trends in Plant Science. 2004. pp. 507–514. 10.1016/j.tplants.2004.08.007 PubMed DOI

Hehenberger E, Kradolfer D, Köhler C. Endosperm cellularization defines an important developmental transition for embryo development. Development. 2012;139: 2031–2039. 10.1242/dev.077057 PubMed DOI

Brink RA, Cooper DC. The endosperm in seed development. Bot Rev. 1947;132: 423–541.

Woodell SRJ, Valentine DH. Studies in british primulas. IX. seed incompatibility in diploid-autotetraploid crosses. New Phytol. 1961;60: 282–294. 10.1111/j.1469-8137.1961.tb06256.x DOI

Ramsey J, Schemske DW. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst. 1998;29: 467–501. 10.1146/annurev.ecolsys.29.1.467 DOI

Lafon-Placette C, Köhler C. Endosperm-based postzygotic hybridization barriers: Developmental mechanisms and evolutionary drivers. Mol Ecol. 2016. 10.1111/mec.13552 PubMed DOI

Ishikawa R, Ohnishi T, Kinoshita Y, Eiguchi M, Kurata N, Kinoshita T. Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J. 2011;65: 798–806. 10.1111/j.1365-313X.2010.04466.x PubMed DOI

Sukno S, Ruso J, Jan CC, Melero-Vara JM, Fernández-Martínez JM. Interspecific hybridization between sunflower and wild perennial Helianthus species via embryo rescue. Euphytica. 1999;106: 69–78. 10.1023/A:1003524822284 DOI

Dinu II, Hayes RJ, Kynast RG, Phillips RL, Thill CA. Novel inter-series hybrids in Solanum, section Petota. Theor Appl Genet. 2005;110: 403–415. 10.1007/s00122-004-1782-x PubMed DOI

Roy AK, Malaviya DR, Kaushal P. Generation of interspecific hybrids of Trifolium using embryo rescue techniques. Methods Mol Biol. 2011;710: 141–151. 10.1007/978-1-61737-988-8_12 PubMed DOI

Lafon-Placette C, Johannessen IM, Hornslien KS, Ali MF, Bjerkan KN, Bramsiepe J, et al. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc Natl Acad Sci U S A. 2017;114: E1027–E1035. 10.1073/pnas.1615123114 PubMed DOI PMC

Tonosaki K, Sekine D, Ohnishi T, Ono A, Furuumi H, Kurata N, et al. Overcoming the species hybridization barrier by ploidy manipulation in the genus Oryza. Plant J. 2018;93: 534–544. 10.1111/tpj.13803 PubMed DOI

Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI. Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci U S A. 2009;106: 5241–5245. 10.1073/pnas.0807679106 PubMed DOI PMC

Guo YL, Bechsgaard JS, Slotte T, Neuffer B, Lascoux M, Weigel D, et al. Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc Natl Acad Sci U S A. 2009;106: 5246–5251. 10.1073/pnas.0808012106 PubMed DOI PMC

Slotte T, Hazzouri KM, Ågren JA, Koenig D, Maumus F, Guo YL, et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat Genet. 2013;45: 831–835. 10.1038/ng.2669 PubMed DOI

Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C. Non-reciprocal interspecies hybridization barriers in the Capsella Genus are established in the endosperm. PLoS Genet. 2015;11 e1005295 10.1371/journal.pgen.1005295 PubMed DOI PMC

Lafon-Placette C, Hatorangan MR, Steige KA, Cornille A, Lascoux M, Slotte T, et al. Paternally expressed imprinted genes associate with hybridization barriers in Capsella. Nat Plants. 2018;4: 352–357. 10.1038/s41477-018-0161-6 PubMed DOI

Scott RJ, Spielman M, Bailey J, Dickinson HG. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998;125: 3329–3341. PubMed

Kradolfer D, Wolff P, Jiang H, Siretskiy A, Köhler C. An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev Cell. 2013;26: 525–535. 10.1016/j.devcel.2013.08.006 PubMed DOI

Jiang H, Moreno-Romero J, Santos-González J, De Jaeger G, Gevaert K, Van De Slijke E, et al. Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation in Arabidopsis thaliana. Genes Dev. 2017;31: 1272–1287. 10.1101/gad.299347.117 PubMed DOI PMC

Wang G, Jiang H, Del Toro de León G, Martinez G, Köhler C. Sequestration of a transposon-derived siRNA by a target mimic imprinted gene induces postzygotic reproductive isolation in Arabidopsis. Dev Cell. 2018;46: 696–705.e4. 10.1016/j.devcel.2018.07.014 PubMed DOI

Batista RA, Moreno-Romero J, Qiu Y, van Boven J, Santos-González J, Figueiredo DD, et al. The MADS-box transcription factor Pheres1 controls imprinting in the endosperm by binding to domesticated transposons. Elife. 2019;8 10.7554/eLife.50541 PubMed DOI PMC

Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM, et al. Imprinting of the Polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet. 2009;5 e1000663 10.1371/journal.pgen.1000663 PubMed DOI PMC

Tiwari S, Spielman M, Schulz R, Oakey RJ, Kelsey G, Salazar A, et al. Transcriptional profiles underlying parent-of-origin effects in seeds of Arabidopsis thaliana. BMC Plant Biol. 2010;10: 72 10.1186/1471-2229-10-72 PubMed DOI PMC

Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L. Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific Incompatibility. Curr Biol. 2009;19: 1128–1132. 10.1016/j.cub.2009.05.068 PubMed DOI PMC

Cao X, Jacobsen SE. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol. 2002;12: 1138–1144. 10.1016/s0960-9822(02)00925-9 PubMed DOI

Zilberman D, Cao X, Jacobsen SE. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 2003;299: 716–719. 10.1126/science.1079695 PubMed DOI

Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. RNA polymerase v transcription guides ARGONAUTE4 to chromatin. Nat Genet. 2009;41: 630–634. 10.1038/ng.365 PubMed DOI PMC

Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol. 2012;22: 1825–1830. 10.1016/j.cub.2012.07.061 PubMed DOI

Moreno-Romero J, Jiang H, Santos-González J, Köhler C. Parental epigenetic asymmetry of PRC 2-mediated histone modifications in the Arabidopsis endosperm. EMBO J. 2016;35: 1298–1311. 10.15252/embj.201593534 PubMed DOI PMC

Grover JW, Kendall T, Baten A, Burgess D, Freeling M, King GJ, et al. Maternal components of RNA-directed DNA methylation are required for seed development in Brassica rapa. Plant J. 2018;94: 575–582. 10.1111/tpj.13910 PubMed DOI

Grover JW, Burgess D, Kendall T, Baten A, Pokhrel S, King GJ, et al. Abundant expression of maternal siRNAs is a conserved feature of seed development. Proc Natl Acad Sci U S A. 2020;117: 202001332 10.1073/pnas.2001332117 PubMed DOI PMC

Koenig D, Hagmann J, Li R, Bemm F, Slotte T, Nueffer B, et al. Long-term balancing selection drives evolution of immunity genes in Capsella. Elife. 2019;8 10.7554/eLife.43606 PubMed DOI PMC

Kasha KJ, Kao KN. High frequency haploid production in barley (Hordeum vulgare L.). Nature. 1970;225: 874–876. 10.1038/225874a0 PubMed DOI

Lange W. Crosses between Hordeum vulgare L. and H. bulbosum L. II. Elimination of chromosomes in hybrid tissues. Euphytica. 1971;20: 181–194. 10.1007/BF00056078 DOI

Bennett MD, Finch RA, Barclay IR. The time rate and mechanism of chromosome elimination in Hordeum hybrids. Chromosom: Springer-Verlag; 1976;54: 175–200. 10.1007/BF00292839 DOI

Sanei M, Pickering R, Kumke K, Nasuda S, Houben A. Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci U S A. 2011;108: E498–E505. 10.1073/pnas.1103190108 PubMed DOI PMC

Hall SE, Luo S, Hall AE, Preuss D. Differential rates of local and global homogenization in centromere satellites from Arabidopsis relatives. Genetics. 2005;170: 1913–1927. 10.1534/genetics.104.038208 PubMed DOI PMC

Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell. 2002;14: 1053–1066. 10.1105/tpc.010425 PubMed DOI PMC

Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science.; 2001. pp. 1098–1102. 10.1126/science.1062939 PubMed DOI

Maheshwari S, Tan EH, West A, Franklin FCH, Comai L, Chan SWL. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genet. 2015;11 e1004970 10.1371/journal.pgen.1004970 PubMed DOI PMC

Du J, Johnson LM, Jacobsen SE, Patel DJ. DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 2015;16: 519–532. 10.1038/nrm4043 PubMed DOI PMC

Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010. pp. 204–220. 10.1038/nrg2719 PubMed DOI PMC

Jullien PE, Berger F. Parental genome dosage imbalance deregulates imprinting in Arabidopsis. PLoS Genet. 2010;6 e1000885 10.1371/journal.pgen.1000885 PubMed DOI PMC

Pařenicová L, De Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, et al. Molecular and phylogenetic analyses of the complete MADS-Box transcription factor family in Arabidopsis: New openings to the MADS world. Plant Cell. 2003;15: 1538–1551. 10.1105/tpc.011544 PubMed DOI PMC

Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science. 2006;314: 1292–1295. 10.1126/science.1133953 PubMed DOI

Thomae AW, Schade GOM, Padeken J, Borath M, Vetter I, Kremmer E, et al. A pair of centromeric proteins mediates reproductive isolation in Drosophila species. Dev Cell. 2013;27: 412–424. 10.1016/j.devcel.2013.10.001 PubMed DOI

Satyaki PRV, Cuykendall TN, Wei KHC, Brideau NJ, Kwak H, Aruna S, et al. The Hmr and Lhr hybrid incompatibility genes suppress a broad range of heterochromatic repeats. PLoS Genet. 2014;10 e1004240 10.1371/journal.pgen.1004240 PubMed DOI PMC

Ferree PM, Barbash DA. Species-Specific Heterochromatin Prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. Noor MAF, editor. PLoS Biol. 2009;7: e1000234 10.1371/journal.pbio.1000234 PubMed DOI PMC

Hurka H, Friesen N, German DA, Franzke A, Neuffer B. ‘Missing link’ species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae). Mol Ecol. 2012;21: 1223–1238. 10.1111/j.1365-294X.2012.05460.x PubMed DOI

Calarco JP, Borges F, Donoghue MTA, Van Ex F, Jullien PE, Lopes T, et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell. 2012;151: 194–205. 10.1016/j.cell.2012.09.001 PubMed DOI PMC

Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science. 2012;337: 1360–1364. 10.1126/science.1224839 PubMed DOI PMC

Schatlowski N, Wolff P, Santos-González J, Schoft V, Siretskiy A, Scott R, et al. Hypomethylated pollen bypasses the interploidy hybridization barrier in Arabidopsis. Plant Cell. 2014;26: 3556–3568. 10.1105/tpc.114.130120 PubMed DOI PMC

Martinez G, Wolff P, Wang Z, Moreno-Romero J, Santos-González J, Conze LL, et al. Paternal easiRNAs regulate parental genome dosage in Arabidopsis. Nat Genet. 2018;50: 193–198. 10.1038/s41588-017-0033-4 PubMed DOI

Zhang W, Lee HR, Koo DH, Jiang J. Epigenetic modification of centromeric chromatin: Hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell. 2008;20: 25–34. 10.1105/tpc.107.057083 PubMed DOI PMC

Doyle J, Doyle F. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987;19:11–15.

Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double Digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 2012;7: e37135 10.1371/journal.pone.0037135 PubMed DOI PMC

Liu X, Karrenberg S. Genetic architecture of traits associated with reproductive barriers in Silene: Coupling, sex chromosomes and variation. Mol Ecol. 2018;27: 3889–3904. 10.1111/mec.14562 PubMed DOI

Steige KA, Reimegård J, Koenig D, Scofield DG, Slotte T. Cis-regulatory changes associated with a recent mating system shift and floral adaptation in Capsella. Mol Biol Evol. 2015;32: 2501–2514. 10.1093/molbev/msv169 PubMed DOI PMC

Eaton DAR. PyRAD: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics. 2014;30: 1844–1849. 10.1093/bioinformatics/btu121 PubMed DOI

Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2 [q-bio.GN] [Preprint]. 2013. Available from: http://www.arxiv-vanity.com/papers/1303.3997/.

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. 10.1101/gr.107524.110 PubMed DOI PMC

Steige KA, Laenen B, Reimegård J, Scofield DG, Slotte T. Genomic analysis reveals major determinants of cis-regulatory variation in Capsella grandiflora. Proc Natl Acad Sci U S A. 2017;114: 1087–1092. 10.1073/pnas.1612561114 PubMed DOI PMC

Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27: 2156–2158. 10.1093/bioinformatics/btr330 PubMed DOI PMC

Quinlan AR, Hall IM, Chen Q, Yang L, Huang H, Miki D, et al. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. 10.1093/bioinformatics/btq033 PubMed DOI PMC

Broman KW, Wu H, Sen Ś, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19: 889–890. 10.1093/bioinformatics/btg112 PubMed DOI

Howey R, Cordell HJ. MapThin: Thinning your map files for linkage analyses! 2011. Available from: http://www.staff.ncl.ac.uk/richard.howey/mapthin/.

Bowler C, Benvenuto G, Laflamme P, Molino D, Probst A V, Tariq M, et al. Chromatin techniques for plant cells. Plant J. 2004;39: 776–789. 10.1111/j.1365-313X.2004.02169.x PubMed DOI

Simon L, Rabanal FA, Dubos T, Oliver C, Lauber D, Poulet A, et al. Genetic and epigenetic variation in 5S ribosomal RNA genes reveals genome dynamics in Arabidopsis thaliana. Nucleic Acids Res. 2018;46: 3019–3033. 10.1093/nar/gky163 PubMed DOI PMC

Trapnell C, Pachter L, Salzberg SL. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25: 1105–1111. 10.1093/bioinformatics/btp120 PubMed DOI PMC

Feng J, Meyer CA, Wang Q, Liu JS, Liu XS, Zhang Y. GFOLD: A generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics. 2012;28: 2782–2788. 10.1093/bioinformatics/bts515 PubMed DOI

Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J. RankProd: A bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics. 2006;22: 2825–2827. 10.1093/bioinformatics/btl476 PubMed DOI

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC

Wang M, Zhao Y, Zhang B. Efficient Test and Visualization of Multi-Set Intersections. Sci Rep. 2015;5: 1–12. 10.1038/srep16923 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...