Ploidy-dependent Changes in the Epigenome of Symbiotic Cells Correlate with Specific Patterns of Gene Expression

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2017 Apr 14

PMID 28404731

Citations 17

Authors

Marianna Nagymihaly

Alaguraj Veluchamy

Zoltan Gyorgypal

Federico Ariel

Teddy Jegu

Moussa Benhamed

Attila Szucs

Attila Kereszt

Peter Mergaert

Eva Kondorosi

Affiliations

Soon will be listed here.

Abstract

The formation of symbiotic nodule cells in is driven by successive endoreduplication cycles and transcriptional reprogramming in different temporal waves including the activation of more than 600 cysteine-rich genes expressed only in nodules. We show here that the transcriptional waves correlate with growing ploidy levels and have investigated how the epigenome changes during endoreduplication cycles. Differential DNA methylation was found in only a small subset of symbiotic nodule-specific genes, including more than half of the genes, whereas in most genes DNA methylation was unaffected by the ploidy levels and was independent of the genes' active or repressed state. On the other hand, expression of nodule-specific genes correlated with ploidy-dependent opening of the chromatin as well as, in a subset of tested genes, with reduced H3K27me3 levels combined with enhanced H3K9ac levels. Our results suggest that endoreduplication-dependent epigenetic changes contribute to transcriptional reprogramming in the differentiation of symbiotic cells.

Citing Articles

Omics-Driven Strategies for Developing Saline-Smart Lentils: A Comprehensive Review.

Ali F, Zhao Y, Ali A, Waseem M, Arif M, Shah O Int J Mol Sci. 2024; 25(21).

PMID: 39518913 PMC: 11546581. DOI: 10.3390/ijms252111360.

Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia.

Nawaz K, Cziesielski M, Mariappan K, Cui G, Aranda M BMC Biol. 2022; 20(1):265.

PMID: 36456984 PMC: 9717517. DOI: 10.1186/s12915-022-01469-y.

Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula.

Knaack S, Conde D, Chakraborty S, Balmant K, Irving T, Maia L BMC Biol. 2022; 20(1):252.

PMID: 36352404 PMC: 9647978. DOI: 10.1186/s12915-022-01450-9.

Polyploidy and Myc Proto-Oncogenes Promote Stress Adaptation via Epigenetic Plasticity and Gene Regulatory Network Rewiring.

Anatskaya O, Vinogradov A Int J Mol Sci. 2022; 23(17).

PMID: 36077092 PMC: 9456078. DOI: 10.3390/ijms23179691.

The Arabidopsis APOLO and human UPAT sequence-unrelated long noncoding RNAs can modulate DNA and histone methylation machineries in plants.

Fonouni-Farde C, Christ A, Blein T, Legascue M, Ferrero L, Moison M Genome Biol. 2022; 23(1):181.

PMID: 36038910 PMC: 9422110. DOI: 10.1186/s13059-022-02750-7.

References

Vinardell J, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z . Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell. 2003; 15(9):2093-105. PMC: 181333. DOI: 10.1105/tpc.014373. View

Pichon M, Journet E, Dedieu A, de Billy F, Truchet G, Barker D . Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell. 1992; 4(10):1199-211. PMC: 160208. DOI: 10.1105/tpc.4.10.1199. View

Xiao T, Schilderink S, Moling S, Deinum E, Kondorosi E, Franssen H . Fate map of Medicago truncatula root nodules. Development. 2014; 141(18):3517-28. DOI: 10.1242/dev.110775. View

Song Q, Lu X, Li Q, Chen H, Hu X, Ma B . Genome-wide analysis of DNA methylation in soybean. Mol Plant. 2013; 6(6):1961-74. DOI: 10.1093/mp/sst123. View

Wildermuth M . Modulation of host nuclear ploidy: a common plant biotroph mechanism. Curr Opin Plant Biol. 2010; 13(4):449-58. DOI: 10.1016/j.pbi.2010.05.005. View

Bramsiepe J, Wester K, Weinl C, Roodbarkelari F, Kasili R, Larkin J . Endoreplication controls cell fate maintenance. PLoS Genet. 2010; 6(6):e1000996. PMC: 2891705. DOI: 10.1371/journal.pgen.1000996. View

Larkins B, Dilkes B, Dante R, Coelho C, Woo Y, Liu Y . Investigating the hows and whys of DNA endoreduplication. J Exp Bot. 2001; 52(355):183-92. View

Lee D, Shin J, Tonge P, Puri M, Lee S, Park H . An epigenomic roadmap to induced pluripotency reveals DNA methylation as a reprogramming modulator. Nat Commun. 2014; 5:5619. PMC: 4284806. DOI: 10.1038/ncomms6619. View

Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan S, Chen H . Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell. 2006; 126(6):1189-201. DOI: 10.1016/j.cell.2006.08.003. View

10.

Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A . A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol. 2003; 132(1):161-73. PMC: 166962. DOI: 10.1104/pp.102.018192. View

11.

Cokus S, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild C . Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008; 452(7184):215-9. PMC: 2377394. DOI: 10.1038/nature06745. View

12.

Vanstraelen M, Baloban M, Da Ines O, Cultrone A, Lammens T, Boudolf V . APC/C-CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc Natl Acad Sci U S A. 2009; 106(28):11806-11. PMC: 2710644. DOI: 10.1073/pnas.0901193106. View

13.

Roh T, Cuddapah S, Zhao K . Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev. 2005; 19(5):542-52. PMC: 551575. DOI: 10.1101/gad.1272505. View

14.

Lister R, OMalley R, Tonti-Filippini J, Gregory B, Berry C, Millar A . Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008; 133(3):523-36. PMC: 2723732. DOI: 10.1016/j.cell.2008.03.029. View

15.

Huang K, Zhang X, Shi J, Yao M, Lin J, Li J . Dynamically reorganized chromatin is the key for the reprogramming of somatic cells to pluripotent cells. Sci Rep. 2015; 5:17691. PMC: 4671053. DOI: 10.1038/srep17691. View

16.

Roux B, Rodde N, Jardinaud M, Timmers T, Sauviac L, Cottret L . An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J. 2014; 77(6):817-37. DOI: 10.1111/tpj.12442. View

17.

Hussein S, Puri M, Tonge P, Benevento M, Corso A, Clancy J . Genome-wide characterization of the routes to pluripotency. Nature. 2014; 516(7530):198-206. DOI: 10.1038/nature14046. View

18.

Maunoury N, Redondo-Nieto M, Bourcy M, Van de Velde W, Alunni B, Laporte P . Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS One. 2010; 5(3):e9519. PMC: 2832008. DOI: 10.1371/journal.pone.0009519. View

19.

Zhou J, Wang X, He K, Charron J, Elling A, Deng X . Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression. Plant Mol Biol. 2010; 72(6):585-95. DOI: 10.1007/s11103-009-9594-7. View

20.

Meissner A, Gnirke A, Bell G, Ramsahoye B, Lander E, Jaenisch R . Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res. 2005; 33(18):5868-77. PMC: 1258174. DOI: 10.1093/nar/gki901. View