Widespread imprinting of transposable elements and variable genes in the maize endosperm

English version

Autoři: Sarah N. Anderson ^aff001; Peng Zhou ^aff002; Kaitlin Higgins ^aff001; Yaniv Brandvain ^aff002; Nathan M. Springer ^aff002
Působiště autorů: Department of Genetics, Development, and Cell Biology; Iowa State University; Ames, Iowa, United States of America ^aff001; Department of Plant and Microbial Biology; University of Minnesota; St. Paul, Minnesota, United States of America ^aff002
Vyšlo v časopise: Widespread imprinting of transposable elements and variable genes in the maize endosperm. PLoS Genet 17(4): e1009491. doi:10.1371/journal.pgen.1009491
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009491

Souhrn

Fertilization and seed development is a critical time in the plant life cycle, and coordinated development of the embryo and endosperm are required to produce a viable seed. In the endosperm, some genes show imprinted expression where transcripts are derived primarily from one parental genome. Imprinted gene expression has been observed across many flowering plant species, though only a small proportion of genes are imprinted. Understanding how imprinted expression arises has been complicated by the reliance on single nucleotide polymorphisms between alleles to enable testing for imprinting. Here, we develop a method to use whole genome assemblies of multiple genotypes to assess for imprinting of both shared and variable portions of the genome using data from reciprocal crosses. This reveals widespread maternal expression of genes and transposable elements with presence-absence variation within maize and across species. Most maternally expressed features are expressed primarily in the endosperm, suggesting that maternal de-repression in the central cell facilitates expression. Furthermore, maternally expressed TEs are enriched for maternal expression of the nearest gene, and read alignments over maternal TE-gene pairs indicate that these are fused rather than independent transcripts.

Klíčová slova:

Endosperm – Gene expression – Genome annotation – Genomic imprinting – Maize – Plant genomics – Single nucleotide polymorphisms – Transposable elements

Zdroje

1. Kermicle JL. Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics. 1970;66: 69–85. 17248508

2. Hsieh T-F, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, et al. Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci U S A. 2011;108: 1755–1762. doi: 10.1073/pnas.1019273108 21257907

3. Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, et al. A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 2011;7: e1002125. doi: 10.1371/journal.pgen.1002125 21731498

4. Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh C-T, Xu W, et al. Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell. 2011;23: 4221–4233. doi: 10.1105/tpc.111.092668 22198147

5. Zhang M, Li N, He W, Zhang H, Yang W, Liu B. Genome-wide screen of genes imprinted in sorghum endosperm, and the roles of allelic differential cytosine methylation. Plant J. 2016;85: 424–436. doi: 10.1111/tpj.13116 26718755

6. Hatorangan MR, Laenen B, Steige KA, Slotte T, Köhler C. Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae. Plant Cell. 2016;28: 1815–1827. doi: 10.1105/tpc.16.00304 27465027

7. Gehring M, Bubb KL, Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science. 2009;324: 1447–1451. doi: 10.1126/science.1171609 19520961

8. Ibarra CA, Feng X, Schoft VK, Hsieh T-F, 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

9. Park K, Kim MY, Vickers M, Park J-S, Hyun Y, Okamoto T, et al. DNA demethylation is initiated in the central cells of Arabidopsis and rice. Proc Natl Acad Sci U S A. 2016;113: 15138–15143. doi: 10.1073/pnas.1619047114 27956642

10. Weinhofer I, Hehenberger E, Roszak P, Hennig L, Köhler C. H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet. 2010;6. doi: 10.1371/journal.pgen.1001152 20949070

11. Moreno-Romero J, Jiang H, Santos-González J, Köhler C. Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm. EMBO J. 2016;35: 1298–1311. doi: 10.15252/embj.201593534 27113256

12. Zhang M, Xie S, Dong X, Zhao X, Zeng B, Chen J, et al. Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genome Res. 2014;24: 167–176. doi: 10.1101/gr.155879.113 24131563

13. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci U S A. 2000;97: 10637–10642. doi: 10.1073/pnas.170292997 10962025

14. Waters AJ, Bilinski P, Eichten SR, Vaughn MW, Ross-Ibarra J, Gehring M, et al. Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc Natl Acad Sci U S A. 2013;110: 19639–19644. doi: 10.1073/pnas.1309182110 24218619

15. Pignatta D, Erdmann RM, Scheer E, Picard CL, Bell GW, Gehring M. Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. Elife. 2014;3: e03198. doi: 10.7554/eLife.03198 24994762

16. Wyder S, Raissig MT, Grossniklaus U. Consistent Reanalysis of Genome-wide Imprinting Studies in Plants Using Generalized Linear Models Increases Concordance across Datasets. Sci Rep. 2019;9: 1320. doi: 10.1038/s41598-018-36768-4 30718537

17. Picard CL, Gehring M. Identification and Comparison of Imprinted Genes Across Plant Species. Methods Mol Biol. 2020;2093: 173–201. doi: 10.1007/978-1-0716-0179-2_13 32088897

18. Springer NM, Ying K, Fu Y, Ji T, Yeh C-T, Jia Y, et al. Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 2009;5: e1000734. doi: 10.1371/journal.pgen.1000734 19956538

19. Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B, et al. Insights into the maize pan-genome and pan-transcriptome. Plant Cell. 2014;26: 121–135. doi: 10.1105/tpc.113.119982 24488960

20. Anderson SN, Stitzer MC, Brohammer AB, Zhou P, Noshay JM, Hirsch CD, et al. Transposable elements contribute to dynamic genome content in maize. The Plant Journal. 2019. doi: 10.1111/tpj.14489 31381222

21. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, et al. Improved maize reference genome with single-molecule technologies. Nature. 2017;546: 524–527. doi: 10.1038/nature22971 28605751

22. Springer NM, Anderson SN, Andorf CM, Ahern KR, Bai F, Barad O, et al. The maize W22 genome provides a foundation for functional genomics and transposon biology. Nat Genet. 2018. doi: 10.1038/s41588-018-0158-0 30061736

23. Hirsch CN, Hirsch CD, Brohammer AB, Bowman MJ, Soifer I, Barad O, et al. Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize. Plant Cell. 2016;28: 2700–2714. doi: 10.1105/tpc.16.00353 27803309

24. Schon MA, Nodine MD. Widespread Contamination of Arabidopsis Embryo and Endosperm Transcriptome Data Sets. Plant Cell. 2017;29: 608–617. doi: 10.1105/tpc.16.00845 28314828

25. Stelpflug SC, Sekhon RS, Vaillancourt B, Hirsch CN, Buell CR, de Leon N, et al. An Expanded Maize Gene Expression Atlas based on RNA Sequencing and its Use to Explore Root Development. Plant Genome. 2016;9. doi: 10.3835/plantgenome2015.04.0025 27898762

26. Portwood JL 2nd, Woodhouse MR, Cannon EK, Gardiner JM, Harper LC, Schaeffer ML, et al. MaizeGDB 2018: the maize multi-genome genetics and genomics database. Nucleic Acids Res. 2019;47: D1146–D1154. doi: 10.1093/nar/gky1046 30407532

27. Schnable JC. Genome evolution in maize: from genomes back to genes. Annu Rev Plant Biol. 2015;66: 329–343. doi: 10.1146/annurev-arplant-043014-115604 25494463

28. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol. 2011;30: 105–111. doi: 10.1038/nbt.2050 22158310

29. Anderson SN, Stitzer MC, Zhou P, Ross-Ibarra J, Hirsch CD, Springer NM. Dynamic Patterns of Transcript Abundance of Transposable Element Families in Maize. G3. 2019;9: 3673–3682. doi: 10.1534/g3.119.400431 31506319

30. 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

31. Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, Nordborg M, et al. Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet. 2008;4: e1000048. doi: 10.1371/journal.pgen.1000048 18389059

32. Warman C, Panda K, Vejlupkova Z, Hokin S, Unger-Wallace E, Cole RA, et al. High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements. PLoS Genet. 2020;16: e1008462. doi: 10.1371/journal.pgen.1008462 32236090

33. Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, et al. Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci U S A. 2011;108: 20042–20047. doi: 10.1073/pnas.1112186108 22114195

34. Anderson SN, Springer NM. Potential roles for transposable elements in creating imprinted expression. Curr Opin Genet Dev. 2018;49: 8–14. doi: 10.1016/j.gde.2018.01.008 29453082

35. Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C, Donoghue MTA, et al. High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis Endosperm. PLoS Genet. 2011;7: e1002126. doi: 10.1371/journal.pgen.1002126 21698132

36. Noshay JM, Anderson SN, Zhou P, Ji L, Ricci W, Lu Z, et al. Monitoring the interplay between transposable element families and DNA methylation in maize. PLoS Genet. 2019;15: e1008291. doi: 10.1371/journal.pgen.1008291 31498837

37. Haig D. Retroviruses and the placenta. Curr Biol. 2012;22: R609–13. doi: 10.1016/j.cub.2012.06.002 22877784

38. Ondičová M, Oakey RJ, Walsh CP. Is imprinting the result of “friendly fire” by the host defense system? PLoS Genet. 2020;16: e1008599. doi: 10.1371/journal.pgen.1008599 32271759

39. Haig D. Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting. Heredity. 2014;113: 96–103. doi: 10.1038/hdy.2013.97 24129605

40. Dilkes BP, Comai L. A differential dosage hypothesis for parental effects in seed development. Plant Cell. 2004;16: 3174–3180. doi: 10.1105/tpc.104.161230 15579806

41. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17: 10–12.

42. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12: 357–360. doi: 10.1038/nmeth.3317 25751142

43. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31: 166–169. doi: 10.1093/bioinformatics/btu638 25260700

44. Zhou P, Hirsch CN, Briggs SP, Springer NM. Dynamic Patterns of Gene Expression Additivity and Regulatory Variation throughout Maize Development. Mol Plant. 2019;12: 410–425. doi: 10.1016/j.molp.2018.12.015 30593858

45. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281

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