Characterization of the DNA accessibility of chloroplast genomes in grasses.

Genome, Chloroplast Poaceae / genetics DNA, Chloroplast / genetics Gene Expression Regulation, Plant Chloroplasts / genetics

Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
22 Jun 2024
Historique:
received: 06 10 2022
accepted: 23 05 2024
medline: 23 6 2024
pubmed: 23 6 2024
entrez: 22 6 2024
Statut: epublish

Résumé

Although the chloroplast genome (cpDNA) of higher plants is known to exist as a large protein-DNA complex called 'plastid nucleoid', researches on its DNA state and regulatory elements are limited. In this study, we performed the assay for transposase-accessible chromatin sequencing (ATAC-seq) on five common tissues across five grasses, and found that the accessibility of different regions in cpDNA varied widely, with the transcribed regions being highly accessible and accessibility patterns around gene start and end sites varying depending on the level of gene expression. Further analysis identified a total of 3970 putative protein binding footprints on cpDNAs of five grasses. These footprints were enriched in intergenic regions and co-localized with known functional elements. Footprints and their flanking accessibility varied dynamically among tissues. Cross-species analysis showed that footprints in coding regions tended to overlap non-degenerate sites and contain a high proportion of highly conserved sites, indicating that they are subject to evolutionary constraints. Taken together, our results suggest that the accessibility of cpDNA has biological implications and provide new insights into the transcriptional regulation of chloroplasts.

Identifiants

DOI: 10.1038/s42003-024-06374-4 PMID: 38909165
pubmed: 38909165
doi: 10.1038/s42003-024-06374-4
pii: 10.1038/s42003-024-06374-4
doi:

Substances chimiques

DNA, Chloroplast 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

760

Subventions

Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : U23A20189
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31922065
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31771755
Organisme : Natural Science Foundation of Hubei Province (Hubei Provincial Natural Science Foundation)
ID : 2023AFA043
Organisme : Earmarked Fund for China Agriculture Research System
ID : CARS-01-01

Informations de copyright

© 2024. The Author(s).

Références

Yagi, Y. & Shiina, T. Recent advances in the study of chloroplast gene expression and its evolution. Front. Plant Sci. 5, 61 (2014).
pubmed: 24611069 pmcid: 3933795 doi: 10.3389/fpls.2014.00061
Daniell, H., Lin, C. S., Yu, M. & Chang, W. J. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 17, 134 (2016).
pubmed: 27339192 pmcid: 4918201 doi: 10.1186/s13059-016-1004-2
Kamimura, Y., Tanaka, H., Kobayashi, Y., Shikanai, T. & Nishimura, Y. Chloroplast nucleoids as a transformable network revealed by live imaging with a microfluidic device. Commun. Biol. 1, 47 (2018).
pubmed: 30271930 pmcid: 6123815 doi: 10.1038/s42003-018-0055-1
Majeran, W. et al. Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol. 158, 156–189 (2012).
pubmed: 22065420 doi: 10.1104/pp.111.188474
Marta P. et al. Dynamic composition, shaping and organization of plastid nucleoids. Front. Plant Sci. 5, 1–13 (2014).
Sato, N. Was the evolution of plastid genetic machinery discontinuous? Trends Plant Sci. 6, 151–155 (2001).
pubmed: 11286919 doi: 10.1016/S1360-1385(01)01888-X
Krupinska, K. et al. WHIRLY1 is a major organizer of chloroplast nucleoids. Front. Plant Sci. 5, 432 (2014).
pubmed: 25237316 pmcid: 4154442 doi: 10.3389/fpls.2014.00432
Kobayashi, Y., Misumi, O., Odahara, M., Ishibashi, K. & Nishimura, Y. Holliday junction resolvases mediate chloroplast nucleoid segregation. Science 356, 631–634 (2017).
pubmed: 28495749 doi: 10.1126/science.aan0038
Kuroiwa T. The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int. Rev. Cytol. 128, 1–62 (1991).
Sakai, A., Takano, H. & Kuroiwa, T. Organelle nuclei in higher plants: structure, composition, function, and evolution. Int. Rev. Cytol. 238, 59–118 (2004).
pubmed: 15364197 doi: 10.1016/S0074-7696(04)38002-2
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213 (2013).
pubmed: 24097267 pmcid: 3959825 doi: 10.1038/nmeth.2688
Buenrostro J. D., Wu B., Chang H. Y., Greenleaf W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.21-29 (2015).
Li, Z. et al. Identification of transcription factor binding sites using ATAC-seq. Genome Biol. 20, 45 (2019).
pubmed: 30808370 pmcid: 6391789 doi: 10.1186/s13059-019-1642-2
Marom, S., Blumberg, A., Kundaje, A. & Mishmar, D. mtDNA chromatin-like organization is gradually established during mammalian embryogenesis. iScience 12, 141–151 (2019).
pubmed: 30684873 pmcid: 6352746 doi: 10.1016/j.isci.2018.12.032
Blumberg, A., Danko, C. G., Kundaje, A. & Mishmar, D. A common pattern of DNase I footprinting throughout the human mtDNA unveils clues for a chromatin-like organization. Genome Res. 28, 1158–1168 (2018).
pubmed: 30002158 pmcid: 6071632 doi: 10.1101/gr.230409.117
Thurman, R. E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75–82 (2012).
pubmed: 22955617 pmcid: 3721348 doi: 10.1038/nature11232
Zhang, W. et al. High-resolution mapping of open chromatin in the rice genome. Genome Res. 22, 151–162 (2012).
Martin, M., Cho, J., Cesare, A. J., Griffith, J. D. & Attardi, G. Termination factor-mediated DNA loop between termination and initiation sites drives mitochondrial rRNA synthesis. Cell 123, 1227–1240 (2005).
pubmed: 16377564 doi: 10.1016/j.cell.2005.09.040
Ding, S. et al. mTERF5 acts as a transcriptional pausing factor to positively regulate transcription of chloroplast psbEFLJ. Mol. Plant 12, 1259–1277 (2019).
pubmed: 31128276 doi: 10.1016/j.molp.2019.05.007
Xiong, H. B. & Wang, J. mTERF8, a member of the mitochondrial transcription termination factor family is involved in the transcription termination of chloroplast gene psbj. Plant Physiol. 182, 408–423 (2020).
pubmed: 31685645 doi: 10.1104/pp.19.00906
Meteignier, L. V. et al. The Arabidopsis mTERF-repeat MDA1 protein plays a dual function in transcription and stabilization of specific chloroplast transcripts within the psbE and ndhH operons. N. Phytol. 227, 1376–1391 (2020).
doi: 10.1111/nph.16625
Zhelyazkova, P. et al. The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24, 123–136 (2012).
Kanno, A. & Hirai, A. A transcription map of the chloroplast genome from rice (Oryza sativa). Curr. Genet. 23, 166–174 (1993).
pubmed: 8381719 doi: 10.1007/BF00352017
Shi, C. et al. Full transcription of the chloroplast genome in photosynthetic eukaryotes. Sci. Rep. 6, 30135 (2016).
pubmed: 27456469 pmcid: 4960489 doi: 10.1038/srep30135
Piper, J. et al. Wellington: a novel method for the accurate identification of digital genomic footprints from DNase-seq data. Nucleic Acids Res. 41, e201 (2013).
pubmed: 24071585 pmcid: 3834841 doi: 10.1093/nar/gkt850
Green, B., Bouchier, C., Fairhead, C., Craig, N. L. & Cormack, B. P. Insertion site preference of Mu, Tn5, and Tn7 transposons. Mob. DNA 3, 3 (2012).
pubmed: 22313799 pmcid: 3292447 doi: 10.1186/1759-8753-3-3
Nordström, K. J. V. et al. Unique and assay specific features of NOMe-, ATAC- and DNase I-seq data. Nucleic Acids Res. 47, 10580–10596 (2019).
pubmed: 31584093 pmcid: 6847574 doi: 10.1093/nar/gkz799
Michalovova, M., Vyskot, B. & Kejnovsky, E. Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization. Heredity 111, 314–320 (2013).
pubmed: 23715017 pmcid: 3807264 doi: 10.1038/hdy.2013.51
Ishizaki, Y. et al. A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 42, 133–144 (2005).
pubmed: 15807777 doi: 10.1111/j.1365-313X.2005.02362.x
Kunnimalaiyaan, M., Shi, F. & Nielsen, B. L. Analysis of the tobacco chloroplast DNA replication origin (oriB) downstream of the 23 S rRNA gene. J. Mol. Biol. 268, 273–283 (1997).
pubmed: 9159470 doi: 10.1006/jmbi.1997.0972
Mühlbauer, S. K., Lössl, A., Tzekova, L., Zou, Z. & Koop, H. U. Functional analysis of plastid DNA replication origins in tobacco by targeted inactivation. Plant J. 32, 175–184 (2002).
pubmed: 12383083 doi: 10.1046/j.1365-313X.2002.01408.x
Oldenburg, D. J. & Bendich, A. J. The linear plastid chromosomes of maize: terminal sequences, structures, and implications for DNA replication. Curr. Genet. 62, 431–442 (2016).
pubmed: 26650613 doi: 10.1007/s00294-015-0548-0
Reyna-Llorens, I. et al. Ancient duons may underpin spatial patterning of gene expression in C4 leaves. Proc. Natl Acad. Sci. USA 115, 1931–1936 (2018).
pubmed: 29432183 pmcid: 5828626 doi: 10.1073/pnas.1720576115
Zhang, Y. et al. A nuclear-encoded protein, mTERF6, mediates transcription termination of rpoA polycistron for plastid-encoded RNA polymerase-dependent chloroplast gene expression and chloroplast development. Sci. Rep. 8, 11929 (2018).
pubmed: 30093718 pmcid: 6085346 doi: 10.1038/s41598-018-30166-6
Burgess, S. J. et al. Genome-wide transcription factor binding in leaves from C3 and C4 grasses. Plant Cell 31, 2297–2314 (2019).
pubmed: 31427470 pmcid: 6790085 doi: 10.1105/tpc.19.00078
Selga, T., Selga, M., Gobiņš, V. & Ozoliņa, A. Plastid-nuclear complexes: permanent structures in photosynthesizing tissues of vascular plants. Laser 25, 000 (2010).
Mahmoud, M. A.-B., Oriane, M., Nate, C. & Karsten, Z. Nucleoid openness profiling links bacterial genome structure to phenotype. Preprint at bioRxiv 2020.2005.2007.082990 (2020).
Zhu, T., Liao, K., Zhou, R., Xia, C. & Xie, W. ATAC-seq with unique molecular identifiers improves quantification and footprinting. Commun. Biol. 3, 675 (2020).
pubmed: 33188264 pmcid: 7666144 doi: 10.1038/s42003-020-01403-4
Zhao, H. et al. An inferred functional impact map of genetic variants in rice. Mol. Plant 14, 1584–1599 (2021).
pubmed: 34214659 doi: 10.1016/j.molp.2021.06.025
Bolger, A. M., Marc, L. & Bjoern, U. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
pubmed: 28263959 pmcid: 5600148 doi: 10.1038/nmeth.4197
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841 (2010).
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690 pmcid: 3603318 doi: 10.1093/molbev/mst010
Pollard, K. S., Hubisz, M. J., Rosenbloom, K. R. & Siepel, A. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res. 20, 110–121 (2010).
pubmed: 19858363 pmcid: 2798823 doi: 10.1101/gr.097857.109
Corbett-Detig, R. B., Hartl, D. L., Sackton, T. B. & Barton, N. H. Natural selection constrains neutral diversity across a wide range of species. PLoS Biol. 13, e1002112 (2015).
pubmed: 25859758 pmcid: 4393120 doi: 10.1371/journal.pbio.1002112

Auteurs

Yinmeng Liu (Y)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China.

Jinling Zhan (J)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China.

Junjie Li (J)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China.

Mengjie Lian (M)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China.

Jiacheng Li (J)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China.

Chunjiao Xia (C)

College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430000, China.

Fei Zhou (F)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China.
College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430000, China.

Weibo Xie (W)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430000, China. weibo.xie@mail.hzau.edu.cn.
Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430000, China. weibo.xie@mail.hzau.edu.cn.
ORCID: 0000-0002-2768-3572

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Classifications MeSH

questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome plastidique › Génome de chloroplaste › Characterization of the DNA accessibility of...
questionsmedicales.fr › Eucaryotes › Viridiplantae › Streptophyta › Embryophyta › Tracheobionta › Magnoliopsida › Poaceae › Characterization of the DNA accessibility of...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › ADN des plantes › ADN des chloroplastes › Characterization of the DNA accessibility of...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Régulation de l'expression des gènes végétaux › Characterization of the DNA accessibility of...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Plastes › Chloroplastes › Characterization of the DNA accessibility of...