Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm
Changes in mating system are supposed to change levels of sexual conflict, causing reduced conflict in inbreeding compared to outbreeding species. The recently diverged species pair of the inbreeding Capsella rubella and the outbreeding C. grandiflora provides the opportunity to test this hypothesis. While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors gave rise to seeds with phenotypic similarities to paternal excess hybridizations in Arabidopsis thaliana, the reciprocal hybridization had similarities to maternal excess hybridizations. These results lend support to the hypothesis that selfing reduces sexual conflict, causing the outcrossing parent to have an increased effective ploidy compared to the selfing parent, resulting in unbalanced genome ratios after hybridization and seed failure. Seed failure correlates with either precocious or delayed endosperm cellularization, in agreement with the endosperm being the battleground for sexual conflict in flowering plants. C. grandiflora and C. rubella have only recently diverged, suggesting that the genes building the hybridization barrier are rapidly evolving as a consequence of sexual conflict.
Vyšlo v časopise:
Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005295
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005295
Souhrn
Changes in mating system are supposed to change levels of sexual conflict, causing reduced conflict in inbreeding compared to outbreeding species. The recently diverged species pair of the inbreeding Capsella rubella and the outbreeding C. grandiflora provides the opportunity to test this hypothesis. While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors gave rise to seeds with phenotypic similarities to paternal excess hybridizations in Arabidopsis thaliana, the reciprocal hybridization had similarities to maternal excess hybridizations. These results lend support to the hypothesis that selfing reduces sexual conflict, causing the outcrossing parent to have an increased effective ploidy compared to the selfing parent, resulting in unbalanced genome ratios after hybridization and seed failure. Seed failure correlates with either precocious or delayed endosperm cellularization, in agreement with the endosperm being the battleground for sexual conflict in flowering plants. C. grandiflora and C. rubella have only recently diverged, suggesting that the genes building the hybridization barrier are rapidly evolving as a consequence of sexual conflict.
Zdroje
1. Guo Y-L, 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. PNAS. 2009;106: 5246–5251. doi: 10.1073/pnas.0808012106 19307580
2. Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI. Recent speciation associated with the evolution of selfing in Capsella. PNAS. 2009;106: 5241–5245. doi: 10.1073/pnas.0807679106 19228944
3. Hurka H, Neuffer B. Evolutionary processes in the genusCapsella (Brassicaceae). Pl Syst Evol. 1997;206: 295–316. doi: 10.1007/BF00987954
4. Paetsch M, Mayland-Quellhorst S, Neuffer B. Evolution of the self-incompatibility system in the Brassicaceae: identification of S-locus receptor kinase (SRK) in self-incompatible Capsella grandiflora. Heredity. 2006;97: 283–290. doi: 10.1038/sj.hdy.6800854 16773120
5. Brandvain Y, Slotte T, Hazzouri KM, Wright SI, Coop G. Genomic Identification of Founding Haplotypes Reveals the History of the Selfing Species Capsella rubella. PLoS Genet. 2013;9: e1003754. doi: 10.1371/journal.pgen.1003754 24068948
6. Brandvain Y, Haig D. Divergent Mating Systems and Parental Conflict as a Barrier to Hybridization in Flowering Plants. The American Naturalist. 2005;166: 330–338. doi: 10.1086/an.2005.166.issue-3 16224688
7. Haig D, Westoby M. Genomic Imprinting in Endosperm: Its Effect on Seed Development in Crosses between Species, and between Different Ploidies of the Same Species, and Its Implications for the Evolution of Apomixis. Phil Trans R Soc Lond B. 1991;333: 1–13. doi: 10.1098/rstb.1991.0057
8. Haig D. GENOMIC IMPRINTING AND KINSHIP: How Good is the Evidence? Annual Review of Genetics. 2004;38: 553–585. doi: 10.1146/annurev.genet.37.110801.142741 15568986
9. Gehring M. Genomic imprinting: insights from plants. Annu Rev Genet. 2013;47: 187–208. doi: 10.1146/annurev-genet-110711-155527 24016190
10. Li J, Berger F. Endosperm: food for humankind and fodder for scientific discoveries. New Phytologist. 2012;195: 290–305. doi: 10.1111/j.1469-8137.2012.04182.x 22642307
11. Boisnard-Lorig C, Colon-Carmona A, Bauch M, Hodge S, Doerner P, Bancharel E, et al. Dynamic Analyses of the Expression of the HISTONE::YFP Fusion Protein in Arabidopsis Show That Syncytial Endosperm Is Divided in Mitotic Domains. Plant Cell. 2001;13: 495–509. doi: 10.1105/tpc.13.3.495 11251092
12. Berger F. Endosperm: the crossroad of seed development. Curr Opin Plant Biol. 2003;6: 42–50. doi: 10.1016/S1369526602000043 12495750
13. Scott RJ, Spielman M, Bailey J, Dickinson HG. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998;125: 3329–3341. 9693137
14. Pignocchi C, Minns GE, Nesi N, Koumproglou R, Kitsios G, Benning C, et al. ENDOSPERM DEFECTIVE1 Is a Novel Microtubule-Associated Protein Essential for Seed Development in Arabidopsis. Plant Cell. 2009;21: 90–105. doi: 10.1105/tpc.108.061812 19151224
15. Hehenberger E, Kradolfer D, Köhler C. Endosperm cellularization defines an important developmental transition for embryo. Development. 2012;139: 2031–2039. doi: 10.1242/dev.077057 22535409
16. Watkins AE. Hybrid sterility and incompatibility. Journ of Genetics. 1932;25: 125–162. doi: 10.1007/BF02983249
17. Cooper DC, Brink RA. The Endosperm as a Barrier to Interspecific Hybridization in Flowering Plants. Science. 1942;95: 75–76. doi: 10.1126/science.95.2455.75 17791072
18. Stebbins GL. The Inviability, Weakness, and Sterility of Interspecific Hybrids. In: Demerec M., editor. Advances in Genetics. Academic Press; 1958. pp. 147–215. 13520442
19. Valentine DH, Woodell SRJ. Seed Incompatibility in Primula. Nature. 1960;185: 778–779. doi: 10.1038/185778b0
20. Bushell C, Spielman M, Scott RJ. The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species. Plant Cell. 2003;15: 1430–1442. 12782734
21. 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. The Plant Journal. 2011;65: 798–806. doi: 10.1111/j.1365-313X.2010.04466.x 21251103
22. Schatlowski N, Köhler C. Tearing down barriers: understanding the molecular mechanisms of interploidy hybridizations. J Exp Bot. 2012;63: 6059–6067. doi: 10.1093/jxb/ers288 23105129
23. Johnston SA, Hanneman RE. Manipulations of Endosperm Balance Number Overcome Crossing Barriers Between Diploid Solanum Species. Science. 1982;217: 446–448. doi: 10.1126/science.217.4558.446 17782980
24. Carputo D, Frusciante L, Peloquin SJ. The Role of 2n Gametes and Endosperm Balance Number in the Origin and Evolution of Polyploids in the Tuber-Bearing Solanums. Genetics. 2003;163: 287–294. 12586716
25. Josefsson C, Dilkes B, Comai L. Parent-Dependent Loss of Gene Silencing during Interspecies Hybridization. Curr Biol. 2006;16: 1322–1328. doi: 10.1016/j.cub.2006.05.045 16824920
26. Gutierrez-Marcos JF, Pennington PD, Costa LM, Dickinson HG. Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos Trans R Soc Lond, B, Biol Sci. 2003;358: 1105–1111. doi: 10.1098/rstb.2003.1292 12831476
27. Birchler JA, Veitia RA. The Gene Balance Hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol. 2010;186: 54–62. doi: 10.1111/j.1469-8137.2009.03087.x 19925558
28. Birchler JA. Interploidy hybridization barrier of endosperm as a dosage interaction. Front Plant Sci. 2014;5: 281. doi: 10.3389/fpls.2014.00281 25018757
29. 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
30. Kradolfer D, Hennig L, Köhler C. Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development. PLoS Genet. 2013;9: e1003163. doi: 10.1371/journal.pgen.1003163 23326241
31. 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; tpc.114.130120. doi: 10.1105/tpc.114.130120
32. D’ Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R. Turning Meiosis into Mitosis. PLoS Biol. 2009;7. doi: 10.1371/journal.pbio.1000124
33. Murata T, Sano T, Sasabe M, Nonaka S, Higashiyama T, Hasezawa S, et al. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat Commun. 2013;4. doi: 10.1038/ncomms2967
34. Xiao C, Somerville C, Anderson CT. POLYGALACTURONASE INVOLVED IN EXPANSION1 Functions in Cell Elongation and Flower Development in Arabidopsis. Plant Cell. 2014;26: 1018–1035. doi: 10.1105/tpc.114.123968 24681615
35. 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
36. Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Mittelsten Scheid O, 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
37. 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 Biology. 2010;10: 72. doi: 10.1186/1471-2229-10-72 20406451
38. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936;21: 113–135. 17246786
39. Muller HJ. Isolating mechanisms, evolution, and temperature. Biol Symp. 1942;6: 71–125.
40. Sicard A, Stacey N, Hermann K, Dessoly J, Neuffer B, Bäurle I, et al. Genetics, Evolution, and Adaptive Significance of the Selfing Syndrome in the Genus Capsella. Plant Cell. 2011;23: 3156–3171. doi: 10.1105/tpc.111.088237 21954462
41. Valentine DH, Woodell SRJ. Studies in British Primulas. X. Seed Incompatibility in Intraspecific and Interspecific Crosses at Diploid and Tetraploid Levels. New Phytol. 1963;62: 125–143.
42. Kato J, Mii M. Production of Interspecific Hybrids in Ornamental Plants. In: Loyola-Vargas VM, Ochoa-Alejo N, editors. Plant Cell Culture Protocols. Humana Press; 2012. pp. 233–245.
43. Garcia D, Fitz Gerald JN, Berger F. Maternal Control of Integument Cell Elongation and Zygotic Control of Endosperm Growth Are Coordinated to Determine Seed Size in Arabidopsis. Plant Cell. 2005;17: 52–60. doi: 10.1105/tpc.104.027136 15598800
44. Sekine D, Ohnishi T, Furuumi H, Ono A, Yamada T, Kurata N, et al. Dissection of two major components of the post-zygotic hybridization barrier in rice endosperm. Plant J. 2013;76: 792–799. doi: 10.1111/tpj.12333 24286595
45. Wagner GK, Pesnot T. Glycosyltransferases and their assays. Chembiochem. 2010;11: 1939–1949. doi: 10.1002/cbic.201000201 20672277
46. Burkart-Waco D, Josefsson C, Dilkes B, Kozloff N, Torjek O, Meyer R, et al. Hybrid incompatibility in Arabidopsis is determined by a multiple-locus genetic network. Plant Physiol. 2012;158: 801–812. doi: 10.1104/pp.111.188706 22135429
47. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, et al. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 2007;5: e236. doi: 10.1371/journal.pbio.0050236 17803357
48. Moyle LC, Nakazato T. Hybrid Incompatibility “Snowballs” Between Solanum Species. Science. 2010;329: 1521–1523. doi: 10.1126/science.1193063 20847271
49. Chae E, Bomblies K, Kim S-T, Karelina D, Zaidem M, Ossowski S, et al. Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis. Cell. 2014;159: 1341–1351. doi: 10.1016/j.cell.2014.10.049 25467443
50. Moyle LC, Graham EB. Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics. 2005;169: 355–373. doi: 10.1534/genetics.104.029546 15466436
51. Fishman L, Willis JH. A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution. 2006;60: 1372–1381. 16929654
52. Sweigart AL, Fishman L, Willis JH. A simple genetic incompatibility causes hybrid male sterility in mimulus. Genetics. 2006;172: 2465–2479. doi: 10.1534/genetics.105.053686 16415357
53. Orr HA, Coyne JA. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics. 1989;121: 527–537. 2714637
54. Coyne JA, Orr HA. “Patterns of Speciation in Drosophila” Revisited. Evolution. 1997;51: 295. doi: 10.2307/2410984
55. Sasa MM, Chippindale PT, Johnson NA. Patterns of Postzygotic Isolation in Frogs. Evolution. 1998;52: 1811. doi: 10.2307/2411351
56. Presgraves DC. Patterns of postzygotic isolation in Lepidoptera. Evolution. 2002;56: 1168–1183. 12144018
57. Roszak P, Köhler C. Polycomb group proteins are required to couple seed coat initiation to fertilization. PNAS. 2011;108: 20826–20831. doi: 10.1073/pnas.1117111108 22143805
58. Simon P. Q-Gene: processing quantitative real-time RT–PCR data. Bioinformatics. 2003;19: 1439–1440. doi: 10.1093/bioinformatics/btg157 12874059
59. Lunter G, Goodson M. Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 2010; doi: 10.1101/gr.111120.110
60. 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
61. Anders S, Pyl PT, Huber W. HTSeq—A Python framework to work with high-throughput sequencing data. bioRxiv. 2014; 002824. doi: 10.1101/002824
62. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. bioRxiv. 2014; 002832. doi: 10.1101/002832
63. Breitling R, Armengaud P, Amtmann A, Herzyk P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Letters. 2004;573: 83–92. doi: 10.1016/j.febslet.2004.07.055 15327980
64. 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
65. Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y. Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol. 2009;150: 535–546. doi: 10.1104/pp.109.136028 19357200
66. Bemer M, Heijmans K, Airoldi C, Davies B, Angenent GC. An Atlas of Type I MADS Box Gene Expression during Female Gametophyte and Seed Development in Arabidopsis. Plant Physiol. 2010;154: 287–300. doi: 10.1104/pp.110.160770 20631316
67. Wang Shengchu, Basten CJ, Zeng Z-B. Windows QTL Cartographer 2.5. In: Department of Statistics, North Carolina State University, Raleigh, NC http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
68. Alexander MP. Differential Staining of Aborted and Nonaborted Pollen. Biotech Histochem. 1969;44: 117–122. doi: 10.3109/10520296909063335
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 6
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm
- Translational Upregulation of an Individual p21 Transcript Variant by GCN2 Regulates Cell Proliferation and Survival under Nutrient Stress
- Exome Sequencing of Phenotypic Extremes Identifies and as Interacting Modifiers of Chronic Infection in Cystic Fibrosis
- The Human Blood Metabolome-Transcriptome Interface