Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm
Autoři:
Katarzyna Dziasek aff001; Lauriane Simon aff001; Clément Lafon-Placette aff001; Benjamin Laenen aff003; Cecilia Wärdig aff001; Juan Santos-González aff001; Tanja Slotte aff003; Claudia Köhler aff001
Působiště autorů:
Department of Plant Biology, Uppsala Biocenter, Swedish University of Agricultural Sciences, Linnean Center of Plant Biology, Uppsala, Sweden
aff001; Present address: Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic
aff002; Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
aff003
Vyšlo v časopise:
Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm. PLoS Genet 17(2): e1009370. doi:10.1371/journal.pgen.1009370
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009370
Souhrn
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.
Klíčová slova:
Arabidopsis thaliana – DNA methylation – Endosperm – Chromatin – Plant genomics – Quantitative trait loci – Seeds – Single nucleotide polymorphisms
Zdroje
1. Li J, Berger F. Endosperm: Food for humankind and fodder for scientific discoveries. New Phytol. 2012;195: 290–305. doi: 10.1111/j.1469-8137.2012.04182.x 22642307
2. 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. doi: 10.1046/j.1365-313x.2002.01491.x 12492846
3. Lin BY. Ploidy barrier to endosperm development in maize. Genetics. 1984;107: 103–15. 17246209
4. 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. doi: 10.1016/j.tplants.2004.08.007 15465686
5. Hehenberger E, Kradolfer D, Köhler C. Endosperm cellularization defines an important developmental transition for embryo development. Development. 2012;139: 2031–2039. doi: 10.1242/dev.077057 22535409
6. Brink RA, Cooper DC. The endosperm in seed development. Bot Rev. 1947;132: 423–541.
7. Woodell SRJ, Valentine DH. Studies in british primulas. IX. seed incompatibility in diploid-autotetraploid crosses. New Phytol. 1961;60: 282–294. doi: 10.1111/j.1469-8137.1961.tb06256.x
8. Ramsey J, Schemske DW. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst. 1998;29: 467–501. doi: 10.1146/annurev.ecolsys.29.1.467
9. Lafon-Placette C, Köhler C. Endosperm-based postzygotic hybridization barriers: Developmental mechanisms and evolutionary drivers. Mol Ecol. 2016. doi: 10.1111/mec.13552 26818717
10. 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. doi: 10.1111/j.1365-313X.2010.04466.x 21251103
11. 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. doi: 10.1023/A:1003524822284
12. 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. doi: 10.1007/s00122-004-1782-x 15517147
13. Roy AK, Malaviya DR, Kaushal P. Generation of interspecific hybrids of Trifolium using embryo rescue techniques. Methods Mol Biol. 2011;710: 141–151. doi: 10.1007/978-1-61737-988-8_12 21207268
14. 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. doi: 10.1073/pnas.1615123114 28115687
15. 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. doi: 10.1111/tpj.13803 29271099
16. 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. doi: 10.1073/pnas.0807679106 19228944
17. 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. doi: 10.1073/pnas.0808012106 19307580
18. 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. doi: 10.1038/ng.2669 23749190
19. 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. doi: 10.1371/journal.pgen.1005295 26086217
20. 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. doi: 10.1038/s41477-018-0161-6 29808019
21. Scott RJ, Spielman M, Bailey J, Dickinson HG. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998;125: 3329–3341. 9693137
22. 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. doi: 10.1016/j.devcel.2013.08.006 24012484
23. 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. doi: 10.1101/gad.299347.117 28743695
24. 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. doi: 10.1016/j.devcel.2018.07.014 30122632
25. 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. doi: 10.7554/eLife.50541 31789592
26. 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. doi: 10.1371/journal.pgen.1000663 19779546
27. 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. doi: 10.1186/1471-2229-10-72 20406451
28. 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. doi: 10.1016/j.cub.2009.05.068 19559614
29. Cao X, Jacobsen SE. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol. 2002;12: 1138–1144. doi: 10.1016/s0960-9822(02)00925-9 12121623
30. Zilberman D, Cao X, Jacobsen SE. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 2003;299: 716–719. doi: 10.1126/science.1079695 12522258
31. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. RNA polymerase v transcription guides ARGONAUTE4 to chromatin. Nat Genet. 2009;41: 630–634. doi: 10.1038/ng.365 19377477
32. 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. doi: 10.1016/j.cub.2012.07.061 22940470
33. 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. doi: 10.15252/embj.201593534 27113256
34. 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. doi: 10.1111/tpj.13910 29569777
35. 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. doi: 10.1073/pnas.2001332117 32541052
36. 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. doi: 10.7554/eLife.43606 30806624
37. Kasha KJ, Kao KN. High frequency haploid production in barley (Hordeum vulgare L.). Nature. 1970;225: 874–876. doi: 10.1038/225874a0 16056782
38. Lange W. Crosses between Hordeum vulgare L. and H. bulbosum L. II. Elimination of chromosomes in hybrid tissues. Euphytica. 1971;20: 181–194. doi: 10.1007/BF00056078
39. Bennett MD, Finch RA, Barclay IR. The time rate and mechanism of chromosome elimination in Hordeum hybrids. Chromosom. Springer-Verlag; 1976;54: 175–200. https://doi.org/10.1007/BF00292839
40. 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. doi: 10.1073/pnas.1103190108 21746892
41. 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. doi: 10.1534/genetics.104.038208 15937135
42. 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. doi: 10.1105/tpc.010425 12034896
43. Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science.; 2001. pp. 1098–1102. doi: 10.1126/science.1062939 11498581
44. 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. doi: 10.1371/journal.pgen.1004970 25622028
45. 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. doi: 10.1038/nrm4043 26296162
46. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010. pp. 204–220. doi: 10.1038/nrg2719 20142834
47. Jullien PE, Berger F. Parental genome dosage imbalance deregulates imprinting in Arabidopsis. PLoS Genet. 2010;6. e1000885. doi: 10.1371/journal.pgen.1000885 20333248
48. 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. doi: 10.1105/tpc.011544 12837945
49. 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. doi: 10.1126/science.1133953 17124320
50. 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. doi: 10.1016/j.devcel.2013.10.001 24239514
51. 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. doi: 10.1371/journal.pgen.1004240 24651406
52. 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. doi: 10.1371/journal.pbio.1000234 19859525
53. 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. doi: 10.1111/j.1365-294X.2012.05460.x 22288429
54. 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. doi: 10.1016/j.cell.2012.09.001 23000270
55. 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. doi: 10.1126/science.1224839 22984074
56. 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. doi: 10.1105/tpc.114.130120 25217506
57. 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. doi: 10.1038/s41588-017-0033-4 29335548
58. 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. doi: 10.1105/tpc.107.057083 18239133
59. Doyle J, Doyle F. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987;19:11–15.
60. 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. doi: 10.1371/journal.pone.0037135 22675423
61. 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. doi: 10.1111/mec.14562 29577481
62. 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. doi: 10.1093/molbev/msv169 26318184
63. Eaton DAR. PyRAD: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics. 2014;30: 1844–1849. doi: 10.1093/bioinformatics/btu121 24603985
64. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404
65. 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/.
66. 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. doi: 10.1101/gr.107524.110 20644199
67. 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. doi: 10.1073/pnas.1612561114 28096395
68. 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. doi: 10.1093/bioinformatics/btr330 21653522
69. 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. doi: 10.1093/bioinformatics/btq033 20110278
70. Broman KW, Wu H, Sen Ś, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19: 889–890. doi: 10.1093/bioinformatics/btg112 12724300
71. Howey R, Cordell HJ. MapThin: Thinning your map files for linkage analyses! 2011. Available from: http://www.staff.ncl.ac.uk/richard.howey/mapthin/.
72. 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. doi: 10.1111/j.1365-313X.2004.02169.x 15315638
73. 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. doi: 10.1093/nar/gky163 29518237
74. Trapnell C, Pachter L, Salzberg SL. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25: 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445
75. 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. doi: 10.1093/bioinformatics/bts515 22923299
76. 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. doi: 10.1093/bioinformatics/btl476 16982708
77. 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. doi: 10.1093/bioinformatics/btp352 19505943
78. Wang M, Zhao Y, Zhang B. Efficient Test and Visualization of Multi-Set Intersections. Sci Rep. 2015;5: 1–12. doi: 10.1038/srep16923 26603754
Článek vyšel v časopise
PLOS Genetics
2021 Číslo 2
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Glucocerebrosidase reduces the spread of protein aggregation in a Drosophila melanogaster model of neurodegeneration by regulating proteins trafficked by extracellular vesicles
- ATF3 downmodulates its new targets IFI6 and IFI27 to suppress the growth and migration of tongue squamous cell carcinoma cells
- Transcriptome-wide transmission disequilibrium analysis identifies novel risk genes for autism spectrum disorder
- Four families of folate-independent methionine synthases