Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler.
Oryza
/ genetics
Genomic Imprinting
Endosperm
/ genetics
Gene Expression Regulation, Plant
DNA Methylation
/ genetics
Chromatin Assembly and Disassembly
/ genetics
Plants, Genetically Modified
DNA Transposable Elements
/ genetics
Plant Proteins
/ genetics
RNA, Small Untranslated
/ genetics
RNA, Plant
/ genetics
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
06 Sep 2024
06 Sep 2024
Historique:
received:
01
09
2023
accepted:
29
08
2024
medline:
7
9
2024
pubmed:
7
9
2024
entrez:
6
9
2024
Statut:
epublish
Résumé
Genomic imprinting is observed in endosperm, a placenta-like seed tissue, where transposable elements (TEs) and repeat-derived small RNAs (sRNAs) mediate epigenetic changes in plants. In imprinting, uniparental gene expression arises due to parent-specific epigenetic marks on one allele but not on the other. The importance of sRNAs and their regulation in endosperm development or in imprinting is poorly understood in crops. Here we show that a previously uncharacterized CLASSY (CLSY)-family chromatin remodeler named OsCLSY3 is essential for rice endosperm development and imprinting, acting as an upstream player in the sRNA pathway. Comparative transcriptome and genetic analysis indicated its endosperm-preferred expression and its likely paternal imprinted nature. These important features are modulated by RNA-directed DNA methylation (RdDM) of tandemly arranged TEs in its promoter. Upon perturbation of OsCLSY3 in transgenic lines, we observe defects in endosperm development and a loss of around 70% of all sRNAs. Interestingly, well-conserved endosperm-specific sRNAs (siren) that are vital for reproductive fitness in angiosperms are also dependent on OsCLSY3. We observed that many imprinted genes and seed development-associated genes are under the control of OsCLSY3. These results support an essential role of OsCLSY3 in rice endosperm development and imprinting, and propose similar regulatory strategies involving CLSY3 homologs among other cereals.
Identifiants
pubmed: 39242590
doi: 10.1038/s41467-024-52239-z
pii: 10.1038/s41467-024-52239-z
doi:
Substances chimiques
DNA Transposable Elements
0
Plant Proteins
0
RNA, Small Untranslated
0
RNA, Plant
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7807Subventions
Organisme : Department of Atomic Energy, Government of India (DAE)
ID : RTI 4006 (1303/3/2019/R&D-II/DAE/4749 dated 16.7.2020
Informations de copyright
© 2024. The Author(s).
Références
Pires, N. D. Seed evolution: parental conflicts in a multi-generational household. Biomol. Concepts 5, 71–86 (2014).
pubmed: 25372743
doi: 10.1515/bmc-2013-0034
Baroux, C., Spillane, C. & Grossniklaus, U. Evolutionary origins of the endosperm in flowering plants. Genome Biol. 3, reviews1026 (2002).
pubmed: 12225592
pmcid: 139410
doi: 10.1186/gb-2002-3-9-reviews1026
Chahtane, H. et al. The plant pathogen Pseudomonas aeruginosa triggers a DELLA-dependent seed germination arrest in Arabidopsis. Elife 7, e37082 (2018).
Iwasaki, M., Hyvärinen, L., Piskurewicz, U. & Lopez-Molina, L. Non-canonical RNA-directed DNA methylation participates in maternal and environmental control of seed dormancy. Elife 8, e37434 (2019).
De Giorgi, J. et al. The Arabidopsis mature endosperm promotes seedling cuticle formation via release of sulfated peptides. Dev. Cell 56, 3066–3081.e5 (2021).
pubmed: 34706263
doi: 10.1016/j.devcel.2021.10.005
Iwasaki, M., Penfield, S. & Lopez-Molina, L. Parental and environmental control of seed dormancy in Arabidopsis thaliana. Annu. Rev. Plant Biol. 73, 355–378 (2022).
pubmed: 35138879
doi: 10.1146/annurev-arplant-102820-090750
Doll, N. M. et al. A two-way molecular dialogue between embryo and endosperm is required for seed development. Science 367, 431–435 (2020).
pubmed: 31974252
doi: 10.1126/science.aaz4131
Li, J. & Berger, F. Endosperm: food for humankind and fodder for scientific discoveries. New Phytol. 195, 290–305 (2012).
pubmed: 22642307
doi: 10.1111/j.1469-8137.2012.04182.x
Gehring, M. Genomic imprinting: insights from plants. Annu. Rev. Genet. 47, 187–208 (2013).
pubmed: 24016190
doi: 10.1146/annurev-genet-110711-155527
Kiyosue, T. et al. Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc. Natl. Acad. Sci. USA 96, 4186–4191 (1999).
pubmed: 10097185
pmcid: 22442
doi: 10.1073/pnas.96.7.4186
Kradolfer, D., Wolff, P., Jiang, H., Siretskiy, A. & Köhler, C. An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev. Cell 26, 525–535 (2013).
pubmed: 24012484
doi: 10.1016/j.devcel.2013.08.006
Gutierrez-Marcos, J. F., Pennington, P. D., Costa, L. M. & Dickinson, H. G. Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1105–1111 (2003).
pubmed: 12831476
pmcid: 1693205
doi: 10.1098/rstb.2003.1292
Kinoshita, T. Reproductive barrier and genomic imprinting in the endosperm of flowering plants. Genes Genet. Syst. 82, 177–186 (2007).
pubmed: 17660688
doi: 10.1266/ggs.82.177
Yuan, J. et al. Both maternally and paternally imprinted genes regulate seed development in rice. New Phytol. 216, 373–387 (2017).
pubmed: 28295376
doi: 10.1111/nph.14510
Gehring, M. et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation Cell. Cell 124, 495–506 (2006).
pubmed: 16469697
pmcid: 4106368
doi: 10.1016/j.cell.2005.12.034
Kinoshita, T. et al. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation Science. Science 303, 521–523 (2004).
pubmed: 14631047
doi: 10.1126/science.1089835
Batista, R. A. & Köhler, C. Genomic imprinting in plants-revisiting existing models. Genes Dev. 34, 24–36 (2020).
pubmed: 31896690
pmcid: 6938664
doi: 10.1101/gad.332924.119
Ishikawa, R. et al. Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J. 65, 798–806 (2011).
pubmed: 21251103
doi: 10.1111/j.1365-313X.2010.04466.x
Huang, F. et al. Mutants in the imprinted PICKLE RELATED 2 gene suppress seed abortion of fertilization independent seed class mutants and paternal excess interploidy crosses in Arabidopsis. Plant J. 90, 383–395 (2017).
pubmed: 28155248
doi: 10.1111/tpj.13500
Zhu, H. et al. DNA demethylase ROS1 negatively regulates the imprinting of DOGL4 and seed dormancy in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 115, E9962–E9970 (2018).
pubmed: 30266793
pmcid: 6196528
doi: 10.1073/pnas.1812847115
Cheng, X. et al. The maternally expressed polycomb group gene OsEMF2a is essential for endosperm cellularization and imprinting in rice. Plant Commun. 2, 100092 (2021).
pubmed: 33511344
doi: 10.1016/j.xplc.2020.100092
Luo, M. et al. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96, 296–301 (1999).
pubmed: 9874812
pmcid: 15133
doi: 10.1073/pnas.96.1.296
Grossniklaus, U., Vielle-Calzada, J. P., Hoeppner, M. A. & Gagliano, W. B. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280, 446–450 (1998).
pubmed: 9545225
doi: 10.1126/science.280.5362.446
Ohad, N. et al. A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93, 5319–5324 (1996).
pubmed: 11607683
pmcid: 39243
doi: 10.1073/pnas.93.11.5319
Waters, A. J. et al. Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc. Natl. Acad. Sci. USA 110, 19639–19644 (2013).
pubmed: 24218619
pmcid: 3845156
doi: 10.1073/pnas.1309182110
Anderson, S. N., Zhou, P., Higgins, K., Brandvain, Y. & Springer, N. M. Widespread imprinting of transposable elements and variable genes in the maize endosperm. PLoS Genet. 17, e1009491 (2021).
pubmed: 33830994
pmcid: 8057601
doi: 10.1371/journal.pgen.1009491
Chen, C. et al. Characterization of imprinted genes in rice reveals conservation of regulation and imprinting with other plant species. Plant Physiol. 177, 1754–1771 (2018).
pubmed: 29914891
pmcid: 6084669
doi: 10.1104/pp.17.01621
Luo, M., Platten, D., Chaudhury, A., Peacock, W. J. & Dennis, E. S. Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol. Plant 2, 711–723 (2009).
pubmed: 19825651
doi: 10.1093/mp/ssp036
Cheng, X. et al. Functional divergence of two duplicated fertilization independent endosperm genes in rice with respect to seed development. Plant J. 104, 124–137 (2020).
pubmed: 33463824
doi: 10.1111/tpj.14911
Köhler, C. & Weinhofer-Molisch, I. Mechanisms and evolution of genomic imprinting in plants. Heredity 105, 57–63 (2010).
pubmed: 19997125
doi: 10.1038/hdy.2009.176
Satyaki, P. R. V. & Gehring, M. DNA methylation and imprinting in plants: machinery and mechanisms. Crit. Rev. Biochem. Mol. Biol. 52, 163–175 (2017).
pubmed: 28118754
doi: 10.1080/10409238.2017.1279119
Stroud, H. et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21, 64–72 (2014).
pubmed: 24336224
doi: 10.1038/nsmb.2735
Smith, L. M. et al. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19, 1507–1521 (2007).
pubmed: 17526749
pmcid: 1913737
doi: 10.1105/tpc.107.051540
Zhang, H. et al. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc. Natl. Acad. Sci. USA 110, 8290–8295 (2013).
pubmed: 23637343
pmcid: 3657815
doi: 10.1073/pnas.1300585110
Law, J. A., Vashisht, A. A., Wohlschlegel, J. A. & Jacobsen, S. E. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7, e1002195 (2011).
pubmed: 21811420
pmcid: 3141008
doi: 10.1371/journal.pgen.1002195
Zhou, M., Palanca, A. M. S. & Law, J. A. Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family. Nat. Genet. 50, 865–873 (2018).
pubmed: 29736015
pmcid: 6317521
doi: 10.1038/s41588-018-0115-y
Zhou, M. et al. The CLASSY family controls tissue-specific DNA methylation patterns in Arabidopsis. Nat. Commun. 13, 244 (2022).
pubmed: 35017514
pmcid: 8752594
doi: 10.1038/s41467-021-27690-x
Martins, L. M. & Law, J. A. Moving targets: mechanisms regulating siRNA production and DNA methylation during plant development. Curr. Opin. Plant Biol. 75, 102435 (2023).
pubmed: 37598540
doi: 10.1016/j.pbi.2023.102435
Vu, T. M. et al. RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140, 2953–2960 (2013).
pubmed: 23760956
pmcid: 3879202
doi: 10.1242/dev.092981
Mosher, R. A. et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460, 283–286 (2009).
pubmed: 19494814
doi: 10.1038/nature08084
Mosher, R. A. Maternal control of Pol IV-dependent siRNAs in Arabidopsis endosperm. New Phytol. 186, 358–364 (2010).
pubmed: 20074090
doi: 10.1111/j.1469-8137.2009.03144.x
Lu, J., Zhang, C., Baulcombe, D. C. & Chen, Z. J. Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 109, 5529–5534 (2012).
pubmed: 22431617
pmcid: 3325730
doi: 10.1073/pnas.1203094109
Kirkbride, R. C. et al. Maternal small RNAs mediate spatial-temporal regulation of gene expression, imprinting, and seed development in Arabidopsis. Proc. Natl. Acad. Sci. USA 116, 2761–2766 (2019).
pubmed: 30692258
pmcid: 6377484
doi: 10.1073/pnas.1807621116
Erdmann, R. M., Satyaki, P. R. V., Klosinska, M. & Gehring, M. A small RNA pathway mediates allelic dosage in endosperm. Cell Rep. 21, 3364–3372 (2017).
pubmed: 29262317
doi: 10.1016/j.celrep.2017.11.078
Xin, M. et al. Dynamic parent-of-origin effects on small interfering RNA expression in the developing maize endosperm. BMC Plant Biol. 14, 192 (2014).
pubmed: 25055833
pmcid: 4222485
doi: 10.1186/s12870-014-0192-8
Grover, J. W. et al. Abundant expression of maternal siRNAs is a conserved feature of seed development. Proc. Natl. Acad. Sci. USA 117, 15305–15315 (2020).
pubmed: 32541052
pmcid: 7334491
doi: 10.1073/pnas.2001332117
Rodrigues, J. A. et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proc. Natl. Acad. Sci. USA 110, 7934–7939 (2013).
pubmed: 23613580
pmcid: 3651473
doi: 10.1073/pnas.1306164110
Burgess, D., Chow, H. T., Grover, J. W., Freeling, M. & Mosher, R. A. Ovule siRNAs methylate protein-coding genes in trans. Plant Cell 34, 3647–3664 (2022).
pubmed: 35781738
pmcid: 9516104
doi: 10.1093/plcell/koac197
Long, J. et al. Nurse cell–derived small RNAs define paternal epigenetic inheritance in Arabidopsis. Science 373, eabh0556 (2021).
pubmed: 34210850
doi: 10.1126/science.abh0556
Olsen, O.-A. The modular control of cereal endosperm development. Trends Plant Sci. 25, 279–290 (2020).
pubmed: 31956036
doi: 10.1016/j.tplants.2019.12.003
Liu, J., Wu, M.-W. & Liu, C.-M. Cereal endosperms: development and storage product accumulation. Annu. Rev. Plant Biol. 73, 255–291 (2022).
pubmed: 35226815
doi: 10.1146/annurev-arplant-070221-024405
Rodrigues, J. A. et al. Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting. Proc. Natl. Acad. Sci. USA 118, e2104445118 (2021).
pubmed: 34272287
pmcid: 8307775
doi: 10.1073/pnas.2104445118
Luo, M. et al. A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 7, e1002125 (2011).
pubmed: 21731498
pmcid: 3121744
doi: 10.1371/journal.pgen.1002125
Waters, A. J. et al. Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23, 4221–4233 (2011).
pubmed: 22198147
pmcid: 3269861
doi: 10.1105/tpc.111.092668
Sato, Y. et al. A rice homeobox gene, OSH1, is expressed before organ differentiation in a specific region during early embryogenesis. Proc. Natl. Acad. Sci. USA 93, 8117–8122 (1996).
pubmed: 8755613
pmcid: 38885
doi: 10.1073/pnas.93.15.8117
Zhiguo, E. et al. A group of nuclear factor Y transcription factors are sub-functionalized during endosperm development in monocots. J. Exp. Bot. 69, 2495–2510 (2018).
doi: 10.1093/jxb/ery087
Li, H. et al. Isolation of five rice nonendosperm tissue-expressed promoters and evaluation of their activities in transgenic rice. Plant Biotechnol. J. 16, 1138–1147 (2018).
pubmed: 29105251
doi: 10.1111/pbi.12858
Hsieh, T.-F. et al. Regulation of imprinted gene expression in Arabidopsis endosperm. Proc. Natl. Acad. Sci. USA 108, 1755–1762 (2011).
pubmed: 21257907
pmcid: 3033266
doi: 10.1073/pnas.1019273108
Le, B. H. et al. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. USA 107, 8063–8070 (2010).
pubmed: 20385809
pmcid: 2889569
doi: 10.1073/pnas.1003530107
Mahto, A., Mathew, I. E. & Agarwal, P. Decoding the transcriptome of rice seed during development. in Advances in Seed Biology (InTech, 2017).
Chen, X. & Zhou, D.-X. Rice epigenomics and epigenetics: challenges and opportunities. Curr. Opin. Plant Biol. 16, 164–169 (2013).
pubmed: 23562565
doi: 10.1016/j.pbi.2013.03.004
Shi, J., Dong, A. & Shen, W.-H. Epigenetic regulation of rice flowering and reproduction. Front. Plant Sci. 5, 803 (2014).
pubmed: 25674094
Higo, A. et al. DNA methylation is reconfigured at the onset of reproduction in rice shoot apical meristem. Nat. Commun. 11, 4079 (2020).
pubmed: 32796936
pmcid: 7429860
doi: 10.1038/s41467-020-17963-2
Wang, L. et al. Reinforcement of CHH methylation through RNA-directed DNA methylation ensures sexual reproduction in rice. Plant Physiol. 188, 1189–1209 (2022).
pubmed: 34791444
doi: 10.1093/plphys/kiab531
Deng, X., Song, X., Wei, L., Liu, C. & Cao, X. Epigenetic regulation and epigenomic landscape in rice. Natl. Sci. Rev. 3, 309–327 (2016).
doi: 10.1093/nsr/nww042
Köhler, C., Page, D. R., Gagliardini, V. & Grossniklaus, U. The Arabidopsis thaliana MEDEA polycomb group protein controls expression of PHERES1 by parental imprinting. Nat. Genet. 37, 28–30 (2005).
pubmed: 15619622
doi: 10.1038/ng1495
Zhang, L. et al. Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24, 4407–4421 (2012).
pubmed: 23150632
pmcid: 3531842
doi: 10.1105/tpc.112.102269
Dhatt, B. K. et al. Allelic variation in rice fertilization independent endosperm 1 contributes to grain width under high night temperature stress. New Phytol. 229, 335–350 (2021).
pubmed: 32858766
doi: 10.1111/nph.16897
Huang, X. et al. Imprinted gene OsFIE1 modulates rice seed development by influencing nutrient metabolism and modifying genome H3K27me3. Plant J. 87, 305–317 (2016).
pubmed: 27133784
doi: 10.1111/tpj.13202
Sun, Q. & Zhou, D.-X. Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc. Natl. Acad. Sci. USA 105, 13679–13684 (2008).
pubmed: 18765808
pmcid: 2533249
doi: 10.1073/pnas.0805901105
Liu, H. et al. OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol. 165, 160–174 (2014).
pubmed: 24596329
pmcid: 4012577
doi: 10.1104/pp.114.235564
Hu, Y. et al. Analysis of rice Snf2 family proteins and their potential roles in epigenetic regulation. Plant Physiol. Biochem. 70, 33–42 (2013).
pubmed: 23770592
doi: 10.1016/j.plaphy.2013.05.001
Yang, D.-L. et al. Four putative SWI2/SNF2 chromatin remodelers have dual roles in regulating DNA methylation in Arabidopsis. Cell Discov. 4, 55 (2018).
pubmed: 30345072
pmcid: 6189096
doi: 10.1038/s41421-018-0056-8
Xu, D., Zeng, L., Wang, L. & Yang, D.-L. Rice requires a chromatin remodeler for polymerase IV-small interfering RNA production and genomic immunity. Plant Physiol. https://doi.org/10.1093/plphys/kiad624 (2023).
Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116–W120 (2005).
pubmed: 15980438
pmcid: 1160203
doi: 10.1093/nar/gki442
Sigrist, C. J. A. et al. PROSITE: a documented database using patterns and profiles as motif descriptors. Brief. Bioinform. 3, 265–274 (2002).
pubmed: 12230035
doi: 10.1093/bib/3.3.265
Musselman, C. A. & Kutateladze, T. G. Characterization of functional disordered regions within chromatin-associated proteins. iScience 24, 102070 (2021).
pubmed: 33604523
pmcid: 7873657
doi: 10.1016/j.isci.2021.102070
Hale, C. J., Stonaker, J. L., Gross, S. M. & Hollick, J. B. A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize. PLoS Biol. 5, e275 (2007).
pubmed: 17941719
pmcid: 2020503
doi: 10.1371/journal.pbio.0050275
Castano-Duque, L., Ghosal, S., Quilloy, F. A., Mitchell-Olds, T. & Dixit, S. An epigenetic pathway in rice connects genetic variation to anaerobic germination and seedling establishment. Plant Physiol. 186, 1042–1059 (2021).
pubmed: 33638990
pmcid: 8195528
doi: 10.1093/plphys/kiab100
Matzke, M. A., Kanno, T. & Matzke, A. J. M. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 66, 243–267 (2015).
pubmed: 25494460
doi: 10.1146/annurev-arplant-043014-114633
Hari Sundar G, V. et al. Plant polymerase IV sensitizes chromatin through histone modifications to preclude spread of silencing into protein-coding domains. Genome Res. https://doi.org/10.1101/gr.277353.122 (2023).
Swetha, C. et al. Major domestication-related phenotypes in Indica rice are due to loss of miRNA-mediated laccase silencing. Plant Cell 30, 2649–2662 (2018).
pubmed: 30341147
pmcid: 6305975
doi: 10.1105/tpc.18.00472
Zilberman, D., Cao, X. & Jacobsen, S. E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716–719 (2003).
pubmed: 12522258
doi: 10.1126/science.1079695
Wu, L. et al. Rice MicroRNA effector complexes and targets. Plant Cell 21, 3421–3435 (2009).
pubmed: 19903869
pmcid: 2798332
doi: 10.1105/tpc.109.070938
Chakraborty, T., Trujillo, J. T., Kendall, T. & Mosher, R. A. A null allele of the pol IV second subunit impacts stature and reproductive development in Oryza sativa. Plant J. 111, 748–755 (2022).
pubmed: 35635763
doi: 10.1111/tpj.15848
Hu, D. et al. Multiplex CRISPR-Cas9 editing of DNA methyltransferases in rice uncovers a class of non-CG methylation specific for GC-rich regions. Plant Cell 33, 2950–2964 (2021).
pubmed: 34117872
pmcid: 8462809
doi: 10.1093/plcell/koab162
Ossowski, S., Schwab, R. & Weigel, D. Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53, 674–690 (2008).
pubmed: 18269576
doi: 10.1111/j.1365-313X.2007.03328.x
Warthmann, N., Chen, H., Ossowski, S., Weigel, D. & Hervé, P. Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3, e1829 (2008).
pubmed: 18350165
pmcid: 2262943
doi: 10.1371/journal.pone.0001829
Narjala, A., Nair, A., Tirumalai, V., Hari Sundar, G. V. & Shivaprasad, P. V. A conserved sequence signature is essential for robust plant miRNA biogenesis. Nucleic Acids Res. 48, 3103–3118 (2020).
pubmed: 32025695
pmcid: 7102948
doi: 10.1093/nar/gkaa077
Zheng, K. et al. The effect of RNA polymerase V on 24-nt siRNA accumulation depends on DNA methylation contexts and histone modifications in rice. Proc. Natl. Acad. Sci. USA 118, e2100709118 (2021).
pubmed: 34290143
pmcid: 8325292
doi: 10.1073/pnas.2100709118
Wolff, P., Jiang, H., Wang, G., Santos-González, J. & Köhler, C. Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. Elife 4, e10074 (2015).
Wang, Z. et al. Polymerase IV plays a crucial role in pollen development in Capsella. Plant Cell 32, 950–966 (2020).
pubmed: 31988265
pmcid: 7145478
doi: 10.1105/tpc.19.00938
Wada, H. et al. Multiple strategies for heat adaptation to prevent chalkiness in the rice endosperm. J. Exp. Bot. 70, 1299–1311 (2019).
pubmed: 30508115
doi: 10.1093/jxb/ery427
An, L. et al. Embryo-endosperm interaction and its agronomic relevance to rice quality. Front. Plant Sci. 11, 587641 (2020).
pubmed: 33424883
pmcid: 7793959
doi: 10.3389/fpls.2020.587641
Yan, D., Duermeyer, L., Leoveanu, C. & Nambara, E. The functions of the endosperm during seed germination. Plant Cell Physiol. 55, 1521–1533 (2014).
pubmed: 24964910
doi: 10.1093/pcp/pcu089
Griffiths-Jones, S., Saini, H. K., van Dongen, S. & Enright, A. J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, D154–D158 (2008).
pubmed: 17991681
doi: 10.1093/nar/gkm952
Anushree, N. & Shivaprasad, P. V. Regulation of plant miRNA biogenesis. In Proc. Indian National Science Academy (A Phys. Sci.) 84, 439–453 (2018).
Hsieh, T.-F. et al. Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451–1454 (2009).
pubmed: 19520962
pmcid: 4044190
doi: 10.1126/science.1172417
Zemach, A. et al. Local DNA hypomethylation activates genes in rice endosperm. Proc. Natl. Acad. Sci. USA 107, 18729–18734 (2010).
pubmed: 20937895
pmcid: 2972920
doi: 10.1073/pnas.1009695107
Li, P. et al. Genes and their molecular functions determining seed structure, components, and quality of rice. Rice 15, 18 (2022).
pubmed: 35303197
pmcid: 8933604
doi: 10.1186/s12284-022-00562-8
Li, N., Xu, R. & Li, Y. Molecular networks of seed size control in plants. Annu. Rev. Plant Biol. 70, 435–463 (2019).
pubmed: 30795704
doi: 10.1146/annurev-arplant-050718-095851
Arora, R. et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8, 242 (2007).
pubmed: 17640358
pmcid: 1947970
doi: 10.1186/1471-2164-8-242
Zhang, J., Nallamilli, B. R., Mujahid, H. & Peng, Z. OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J. 64, 604–617 (2010).
pubmed: 20822505
doi: 10.1111/j.1365-313X.2010.04354.x
Paul, P. et al. MADS78 and MADS79 are essential regulators of early seed development in rice. Plant Physiol. 182, 933–948 (2020).
pubmed: 31818903
doi: 10.1104/pp.19.00917
Chen, C. et al. Heat stress yields a unique MADS box transcription factor in determining seed size and thermal sensitivity. Plant Physiol. 171, 606–622 (2016).
pubmed: 26936896
pmcid: 4854699
doi: 10.1104/pp.15.01992
Zhang, H., Xu, H., Feng, M. & Zhu, Y. Suppression of OsMADS7 in rice endosperm stabilizes amylose content under high temperature stress. Plant Biotechnol. J. 16, 18–26 (2018).
pubmed: 28429576
doi: 10.1111/pbi.12745
Jiang, H. & Köhler, C. Evolution, function, and regulation of genomic imprinting in plant seed development. J. Exp. Bot. 63, 4713–4722 (2012).
pubmed: 22922638
doi: 10.1093/jxb/ers145
Tonosaki, K. et al. Mutation of the imprinted gene OsEMF2a induces autonomous endosperm development and delayed cellularization in rice. Plant Cell 33, 85–103 (2021).
pubmed: 33751094
Xiao, W. et al. Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev. Cell 5, 891–901 (2003).
pubmed: 14667411
doi: 10.1016/S1534-5807(03)00361-7
Kim, M. Y. et al. DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm. Proc. Natl. Acad. Sci. USA 116, 9652–9657 (2019).
pubmed: 31000601
pmcid: 6511055
doi: 10.1073/pnas.1821435116
Chow, H. T. & Mosher, R. A. Small RNA-mediated DNA methylation during plant reproduction. Plant Cell 35, 1787–1800 (2023).
pubmed: 36651080
pmcid: 10226566
doi: 10.1093/plcell/koad010
Grover, J. W. et al. Maternal components of RNA-directed DNA methylation are required for seed development in Brassica rapa. Plant J. 94, 575–582 (2018).
pubmed: 29569777
doi: 10.1111/tpj.13910
Shahzad, Z., Eaglesfield, R., Carr, C. & Amtmann, A. Cryptic variation in RNA-directed DNA-methylation controls lateral root development when auxin signalling is perturbed. Nat. Commun. 11, 218 (2020).
pubmed: 31924796
pmcid: 6954204
doi: 10.1038/s41467-019-13927-3
Quesneville, H. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mob. DNA 11, 28 (2020).
pubmed: 32742313
pmcid: 7385966
doi: 10.1186/s13100-020-00223-x
Kinoshita, Y. et al. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49, 38–45 (2007).
pubmed: 17144899
doi: 10.1111/j.1365-313X.2006.02936.x
Williams, B. P., Pignatta, D., Henikoff, S. & Gehring, M. Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat. PLoS Genet. 11, e1005142 (2015).
pubmed: 25826366
pmcid: 4380477
doi: 10.1371/journal.pgen.1005142
Batista, R. A. et al. The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons. Elife 8, e50541 (2019).
Nosaka, M. et al. Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet. 8, e1002953 (2012).
pubmed: 23028360
pmcid: 3459959
doi: 10.1371/journal.pgen.1002953
Xu, L. et al. Regulation of rice tillering by RNA-directed DNA methylation at miniature inverted-repeat transposable elements. Mol. Plant 13, 851–863 (2020).
pubmed: 32087371
doi: 10.1016/j.molp.2020.02.009
Shen, J. et al. Translational repression by a miniature inverted-repeat transposable element in the 3′ untranslated region. Nat. Commun. 8, 14651 (2017).
pubmed: 28256530
pmcid: 5338036
doi: 10.1038/ncomms14651
Jullien, P. E., Katz, A., Oliva, M., Ohad, N. & Berger, F. Polycomb group complexes self-regulate imprinting of the polycomb group gene MEDEA in Arabidopsis. Curr. Biol. 16, 486–492 (2006).
pubmed: 16527743
doi: 10.1016/j.cub.2006.01.020
Satyaki, P. R. V. & Gehring, M. RNA Pol IV induces antagonistic parent-of-origin effects on Arabidopsis endosperm. PLoS Biol. 20, e3001602 (2022).
pubmed: 35389984
pmcid: 9017945
doi: 10.1371/journal.pbio.3001602
Hu, X. et al. The U-box E3 ubiquitin ligase TUD1 functions with a heterotrimeric G α subunit to regulate brassinosteroid-mediated growth in rice. PLoS Genet. 9, e1003391 (2013).
pubmed: 23526892
pmcid: 3597501
doi: 10.1371/journal.pgen.1003391
Gao, X. et al. Rice qGL3/OsPPKL1 functions with the GSK3/SHAGGY-like kinase OsGSK3 to modulate brassinosteroid signaling. Plant Cell 31, 1077–1093 (2019).
pubmed: 30923230
pmcid: 6533024
doi: 10.1105/tpc.18.00836
Qin, R. et al. LTBSG1, a new allele of BRD2, regulates panicle and grain development in rice by brassinosteroid biosynthetic pathway. Genes 9, 292 (2018).
pubmed: 29891831
pmcid: 6027417
doi: 10.3390/genes9060292
Huang, J. et al. Natural variation of the BRD2 allele affects plant height and grain size in rice. Planta 256, 27 (2022).
pubmed: 35780402
doi: 10.1007/s00425-022-03939-7
Liu, Z. et al. OsMKKK70 regulates grain size and leaf angle in rice through the OsMKK4-OsMAPK6-OsWRKY53 signaling pathway. J. Integr. Plant Biol. 63, 2043–2057 (2021).
pubmed: 34561955
doi: 10.1111/jipb.13174
Xu, R. et al. Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol. Plant 11, 860–873 (2018).
pubmed: 29702261
doi: 10.1016/j.molp.2018.04.004
Yin, L.-L. & Xue, H.-W. The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24, 1049–1065 (2012).
pubmed: 22408076
pmcid: 3336122
doi: 10.1105/tpc.111.094854
Nayar, S., Sharma, R., Tyagi, A. K. & Kapoor, S. Functional delineation of rice MADS29 reveals its role in embryo and endosperm development by affecting hormone homeostasis. J. Exp. Bot. 64, 4239–4253 (2013).
pubmed: 23929654
pmcid: 3808311
doi: 10.1093/jxb/ert231
Nayar, S., Kapoor, M. & Kapoor, S. Post-translational regulation of rice MADS29 function: homodimerization or binary interactions with other seed-expressed MADS proteins modulate its translocation into the nucleus. J. Exp. Bot. 65, 5339–5350 (2014).
pubmed: 25096923
pmcid: 4157715
doi: 10.1093/jxb/eru296
Tang, J., Mei, E., He, M., Bu, Q. & Tian, X. Functions of OsWRKY24, OsWRKY70 and OsWRKY53 in regulating grain size in rice. Planta 255, 92 (2022).
pubmed: 35322309
doi: 10.1007/s00425-022-03871-w
Ogawa, D. et al. RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice. Nat. Commun. 2, 278 (2011).
pubmed: 21505434
doi: 10.1038/ncomms1279
Tiwari, G. J., Liu, Q., Shreshtha, P., Li, Z. & Rahman, S. RNAi-mediated down-regulation of the expression of OsFAD2-1: effect on lipid accumulation and expression of lipid biosynthetic genes in the rice grain. BMC Plant Biol. 16, 1–13 (2016).
Yang, J., Luo, D., Yang, B., Frommer, W. B. & Eom, J.-S. SWEET11 and 15 as key players in seed filling in rice. New Phytol. 218, 604–615 (2018).
pubmed: 29393510
doi: 10.1111/nph.15004
Peng, B. et al. Scanning electron microscopic observation on chalkiness of rice mutant OsLHT1 grains. J. Agric. Sci. 14, 54 (2022).
Liu, Z. et al. Transcription factor OsSGL is a regulator of starch synthesis and grain quality in rice. J. Exp. Bot. 73, 3417–3430 (2022).
pubmed: 35182423
doi: 10.1093/jxb/erac068
Xie, K. & Yang, Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 6, 1975–1983 (2013).
pubmed: 23956122
doi: 10.1093/mp/sst119
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10 (2011).
doi: 10.14806/ej.17.1.200
Clement, K. et al. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat. Biotechnol. 37, 224–226 (2019).
pubmed: 30809026
pmcid: 6533916
doi: 10.1038/s41587-019-0032-3
Wang, G., Wang, G., Zhang, X., Wang, F. & Song, R. Isolation of high quality RNA from cereal seeds containing high levels of starch. Phytochem. Anal. 23, 159–163 (2012).
pubmed: 21739496
doi: 10.1002/pca.1337
Shivaprasad, P. V., Dunn, R. M., Santos, B. A., Bassett, A. & Baulcombe, D. C. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31, 257–266 (2012).
pubmed: 22179699
doi: 10.1038/emboj.2011.458
Tirumalai, V., Prasad, M. & Shivaprasad, P. V. RNA blot analysis for the detection and quantification of plant microRNAs. J. Vis. Exp. https://doi.org/10.3791/61394 (2020).
Ramanathan, V. & Veluthambi, K. Transfer of non-T-DNA portions of the Agrobacterium tumefaciens Ti plasmid pTiA6 from the left terminus of TL-DNA. Plant Mol. Biol. 28, 1149–1154 (1995).
pubmed: 7548833
doi: 10.1007/BF00032676
Vivek Hari Sundar, G. & Shivaprasad, P. V. Investigation of transposon DNA methylation and copy number variation in plants using southern hybridisation. Bio Protoc. 12, e4432 (2022).
Rogers, S. O. & Bendich, A. J. Extraction of total cellular DNA from plants, algae and fungi. in Plant Molecular Biology Manual 183–190 (Springer Netherlands, Dordrecht, 1994).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics 27, 1571–1572 (2011).
pubmed: 21493656
pmcid: 3102221
doi: 10.1093/bioinformatics/btr167
Huang, X., Zhang, S., Li, K., Thimmapuram, J. & Xie, S. ViewBS: a powerful toolkit for visualization of high-throughput bisulfite sequencing data. Bioinformatics 34, 708–709 (2018).
pubmed: 29087450
doi: 10.1093/bioinformatics/btx633
Stocks, M. B. et al. The UEA sRNA Workbench (version 4.4): a comprehensive suite of tools for analyzing miRNAs and sRNAs. Bioinformatics 34, 3382–3384 (2018).
pubmed: 29722807
pmcid: 6157081
doi: 10.1093/bioinformatics/bty338
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
pubmed: 19261174
pmcid: 2690996
doi: 10.1186/gb-2009-10-3-r25
Axtell, M. J. ShortStack: comprehensive annotation and quantification of small RNA genes. RNA 19, 740–751 (2013).
pubmed: 23610128
pmcid: 3683909
doi: 10.1261/rna.035279.112
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
Quinlan, A. R. BEDTools: the Swiss-army tool for genome feature analysis. Curr. Protoc. Bioinform. 47, 11.12.1–34 (2014).
doi: 10.1002/0471250953.bi1112s47
Wickham, H. Ggplot2 (Springer International Publishing, Cham, Switzerland, 2016).
Khan, A. & Mathelier, A. Intervene: a tool for intersection and visualization of multiple gene or genomic region sets. BMC Bioinform. 18, 1–8 (2017).
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142
pmcid: 4655817
doi: 10.1038/nmeth.3317
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
pubmed: 22383036
pmcid: 3334321
doi: 10.1038/nprot.2012.016
Patwardhan, M. N., Wenger, C. D., Davis, E. S., Phanstiel, D. H. & Bedtoolsr An R package for genomic data analysis and manipulation. J. Open Source Softw. 4, 1742 (2019).
pubmed: 31903447
pmcid: 6941791
doi: 10.21105/joss.01742
Song, L., Koga, Y. & Ecker, J. R. Profiling of transcription factor binding events by chromatin immunoprecipitation sequencing (ChIP-seq). Curr. Protoc. Plant Biol. 1, 293–306 (2016).
pubmed: 28782043
pmcid: 5544034
doi: 10.1002/cppb.20014
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975
pmcid: 4987876
doi: 10.1093/nar/gkw257
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187–W191 (2014).
pubmed: 24799436
pmcid: 4086134
doi: 10.1093/nar/gku365
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982
pmcid: 2592715
doi: 10.1186/gb-2008-9-9-r137
Ge, S. X., Jung, D. & Yao, R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36, 2628–2629 (2020).
pubmed: 31882993
doi: 10.1093/bioinformatics/btz931
Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987).
pubmed: 3327686
pmcid: 553867
doi: 10.1002/j.1460-2075.1987.tb02730.x
Shariq, M. et al. Adult neural stem cells have latent inflammatory potential that is kept suppressed by Tcf4 to facilitate adult neurogenesis. Sci. Adv. 7, eabf5606 (2021).
pubmed: 34020954
pmcid: 8139598
doi: 10.1126/sciadv.abf5606
Pachamuthu, K. et al. Rice-specific Argonaute 17 controls reproductive growth and yield-associated phenotypes. Plant Mol. Biol. 105, 99–114 (2021).
pubmed: 32964370
doi: 10.1007/s11103-020-01071-2
He, Y. et al. Indole-3-acetate beta-glucosyltransferase OsIAGLU regulates seed vigour through mediating crosstalk between auxin and abscisic acid in rice. Plant Biotechnol. J. 18, 1933–1945 (2020).
pubmed: 32012429
pmcid: 7415787
doi: 10.1111/pbi.13353
Khatun, S. & Flowers, T. J. The estimation of pollen viability in rice. J. Exp. Bot. 46, 151–154 (1995).
doi: 10.1093/jxb/46.1.151
Yao, M. et al. Downregulation of OsAGO17 by artificial microRNA causes pollen abortion resulting in the reduction of grain yield in rice. Electron. J. Biotechnol. https://doi.org/10.1016/j.ejbt.2018.07.001 (2018).
Das, S., Swetha, C., Pachamuthu, K., Nair, A. & Shivaprasad, P. V. Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs. Plant Reprod. 33, 59–73 (2020).
pubmed: 32157461
doi: 10.1007/s00497-020-00386-w