Stocktake Sale on now: wide range of books at up to 70% off!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

DELAY OF GERMINATION 1 (DOG1) regulates dormancy in dimorphic seeds of Xanthium strumarium

Iman Nemati A , Mohammad Sedghi https://orcid.org/0000-0001-5969-1860 A * , Ghasem Hosseini Salekdeh B C , Reza Tavakkol Afshari D , Mohammad Reza Naghavi E and Somayeh Gholizadeh F
+ Author Affiliations
- Author Affiliations

A Department of Plant Production and Genetics Engineering, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

B Department of Molecular Sciences, Macquarie University, Sydney, NSW 2109, Australia.

C Department of Systems and Synthetic Biology, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran.

D Department of Agronomy, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.

E Agricultural and Natural Resources College, University of Tehran, Tehran, Iran.

F Department of Plant Breeding and Biotechnology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran.

* Correspondence to: m_sedghi@uma.ac.ir

Handling Editor: Peter Bozhkov

Functional Plant Biology 49(8) 742-758 https://doi.org/10.1071/FP21315
Submitted: 12 June 2021  Accepted: 23 March 2022   Published: 16 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Seed dormancy ensures plant survival but many mechanisms remain unclear. A high-throughput RNA-seq analysis investigated the mechanisms involved in the establishment of dormancy in dimorphic seeds of Xanthium strumarium (L.) developing in one single burr. Results showed that DOG1, the main dormancy gene in Arabidopsis thaliana L., was over-represented in the dormant seed leading to the formation of two seeds with different cell wall properties. Less expression of DME/EMB1649, UBP26, EMF2, MOM, SNL2, and AGO4 in the non-dormant seed was observed, which function in the chromatin remodelling of dormancy-associated genes through DNA methylation. However, higher levels of ATXR7/SDG25, ELF6, and JMJ16/PKDM7D in the non-dormant seed that act at the level of histone demethylation and activate germination were found. Dramatically lower expression in the splicing factors SUA, PWI, and FY in non-dormant seed may indicate that variation in RNA splicing for ABA sensitivity and transcriptional elongation control of DOG1 is of importance for inducing seed dormancy. Seed size and germination may be influenced by respiratory factors, and alterations in ABA content and auxin distribution and responses. TOR (a serine/threonine-protein kinase) is likely at the centre of a regulatory hub controlling seed metabolism, maturation, and germination. Over-representation of the respiration-associated genes (ACO3, PEPC3, and D2HGDH) was detected in non-dormant seed, suggesting differential energy supplies in the two seeds. Degradation of ABA biosynthesis and/or proper auxin signalling in the large seed may control germinability, and suppression of endoreduplication in the small seed may be a mechanism for cell differentiation and cell size determination.

Keywords: ABA, DOG1, dormancy, germination, phytohormone, respiration, transcriptome, Xanthium strumarium.


References

Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Frontiers in Plant Science 4, 63
ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination.Crossref | GoogleScholarGoogle Scholar | 23531630PubMed |

Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942.
A central integrator of transcription networks in plant stress and energy signalling.Crossref | GoogleScholarGoogle Scholar | 17671505PubMed |

Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 17042–17047.
Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17065317PubMed |

Broeckx T, Hulsmans S, Rolland F (2016) The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function. Journal of Experimental Botany 67, 6215–6252.
The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function.Crossref | GoogleScholarGoogle Scholar | 27856705PubMed |

Chen H, Tong J, Fu W, Liang Z, Ruan J, Yu Y, et al. (2020) The H3K27me3 demethylase RELATIVE OF EARLY FLOWERING6 suppresses seed dormancy by inducing abscisic acid catabolism. Plant Physiology 184, 1969–1978.
The H3K27me3 demethylase RELATIVE OF EARLY FLOWERING6 suppresses seed dormancy by inducing abscisic acid catabolism.Crossref | GoogleScholarGoogle Scholar | 33037128PubMed |

Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, et al. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42.
DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12150995PubMed |

Cyrek M, Fedak H, Ciesielski A, Guo Y, Sliwa A, Brzezniak L, et al. (2016) Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1. Plant Physiology 170, 947–955.
Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1.Crossref | GoogleScholarGoogle Scholar | 26620523PubMed |

Dekkers BJW, He H, Hanson J, Willems LAJ, Jamar DCL, Cueff G, et al. (2016) The Arabidopsis DELAY Of GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. The Plant Journal 85, 451–465.
The Arabidopsis DELAY Of GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development.Crossref | GoogleScholarGoogle Scholar |

Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, et al. (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. The Plant Cell 20, 3006–3021.
A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 18984676PubMed |

Ferraz dos Santos L, Santana Silva RJ, Oliveira Jordão do Amaral D, Barbosa de Paula MF, Falcão Ludke L, Legavre T, et al. (2016) Selection of reference genes for expression study in pulp and seeds of Theobroma Grandiflorum (Willd. Ex Spreng.) Schum. PLoS ONE 11, e0160646
Selection of reference genes for expression study in pulp and seeds of Theobroma Grandiflorum (Willd. Ex Spreng.) Schum.Crossref | GoogleScholarGoogle Scholar | 27501324PubMed |

Franciosini A, Moubayidin L, Du K, Matari NH, Boccaccini A, Butera S, et al. (2015) The COP9 SIGNALOSOME is required for postembryonic meristem maintenance in Arabidopsis thaliana. Molecular Plant 8, 1623–1634.
The COP9 SIGNALOSOME is required for postembryonic meristem maintenance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 26277260PubMed |

Fu L, Wang P, Xiong Y (2020) Target of rapamycin signaling in plant stress responses. Plant Physiology 182, 1613–1623.
Target of rapamycin signaling in plant stress responses.Crossref | GoogleScholarGoogle Scholar | 31949028PubMed |

Ghelis T, Bolbach G, Clodic G, Habricot Y, Miginiac E, Sotta B, Jeannette E (2008) Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells. Plant Physiology 148, 1668–1680.
Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells.Crossref | GoogleScholarGoogle Scholar | 18768909PubMed |

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652.
Full-length transcriptome assembly from RNA-Seq data without a reference genome.Crossref | GoogleScholarGoogle Scholar | 21572440PubMed |

Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell & Environment 35, 1769–1786.
Molecular mechanisms of seed dormancy.Crossref | GoogleScholarGoogle Scholar |

Graeber K, Linkies A, Steinbrecher T, Mummenhoff K, Tarkowská D, Turečková V, et al. (2014) DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination. Proceedings of the National Academy of Sciences of the United States of America 111, E3571–E3580.
DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination.Crossref | GoogleScholarGoogle Scholar | 25114251PubMed |

Grubb CD, Zipp BJ, Ludwig-Muller J, Masuno MN, Molinski TF, Abel S (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. The Plant Journal 40, 893–908.
Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis.Crossref | GoogleScholarGoogle Scholar | 15584955PubMed |

Heyman J, Canher B, Bisht A, Christiaens F, De Veylder L (2018) Emerging role of the plant erf transcription factors in coordinating wound defense responses and repair. Journal of Cell Science 131, jcs208215
Emerging role of the plant erf transcription factors in coordinating wound defense responses and repair.Crossref | GoogleScholarGoogle Scholar | 29242229PubMed |

Hu Y, Yu D (2014) BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. The Plant Cell 26, 4394–4408.
BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25415975PubMed |

Huang H, Quint M, Gray WM (2013) The eta7/csn3-3 auxin response mutant of Arabidopsis defines a novel function for the CSN3 subunit of the COP9 signalosome. PLoS ONE 8, e66578
The eta7/csn3-3 auxin response mutant of Arabidopsis defines a novel function for the CSN3 subunit of the COP9 signalosome.Crossref | GoogleScholarGoogle Scholar | 23762492PubMed |

Huo H, Wei S, Bradford KJ (2016) DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proceedings of the National Academy of Sciences of the United States of America 113, E2199–E2206.
DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways.Crossref | GoogleScholarGoogle Scholar | 27035986PubMed |

Irigoyen ML, Iniesto E, Rodriguez L, Puga MI, Yanagawa Y, Pick E, et al. (2014) Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. The Plant Cell 26, 712–728.
Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24563205PubMed |

Jaiswal PS, Kaur N, Randhawa GS (2019) Identification of reference genes for QRT-PCR gene expression studies during seed development and under abiotic stresses in Cyamopsis tetragonoloba. Crop Science 59, 252–265.
Identification of reference genes for QRT-PCR gene expression studies during seed development and under abiotic stresses in Cyamopsis tetragonoloba.Crossref | GoogleScholarGoogle Scholar |

Jiang S, Kumar S, Eu Y-J, Jami SK, Stasolla C, Hill RD (2012) The Arabidopsis mutant, fy-1, has an ABA-insensitive germination phenotype. Journal of Experimental Botany 63, 2693–2703.
The Arabidopsis mutant, fy-1, has an ABA-insensitive germination phenotype.Crossref | GoogleScholarGoogle Scholar | 22282534PubMed |

Jin D, Wu M, Li B, Bucker B, Keli P, Zhang S, et al. (2018) The COP9 Signalosome regulates seed germination by facilitating protein degradation of RGL2 and ABI5. PLOS Genetics 14, e1007237
The COP9 Signalosome regulates seed germination by facilitating protein degradation of RGL2 and ABI5.Crossref | GoogleScholarGoogle Scholar | 29462139PubMed |

Katoh H, Esashi Y (1975) Dormancy and impotency of cocklebur seeds I. CO2, C2H4O2, and high temperature. Plant and Cell Physiology 16, 687–696.
Dormancy and impotency of cocklebur seeds I. CO2, C2H4O2, and high temperature.Crossref | GoogleScholarGoogle Scholar |

Kim DH, Sung S (2014) Polycomb-mediated gene silencing in Arabidopsis thaliana. Molecular Cells 37, 841–850.
Polycomb-mediated gene silencing in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Kim SY, Zhu T, Renee Sung Z (2010) Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiology 152, 516–528.
Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19783648PubMed |

Kim S, Park JS, Lee J, Lee KK, Park OS, Choi HS, Seo PJ, Cho HT, Frost JM, Fischer RL, Choi Y (2021) The DME demethylase regulates sporophyte gene expression, cell proliferation, differentiation, and meristem resurrection. Proceedings of the National Academy of Sciences of the United States of America 118, e2026806118
The DME demethylase regulates sporophyte gene expression, cell proliferation, differentiation, and meristem resurrection.Crossref | GoogleScholarGoogle Scholar | 34266952PubMed |

Klupczyńska EA, Pawłowski TA (2021) Regulation of seed dormancy and germination mechanisms in a changing environment. International Journal of Molecular Sciences 22, 1357
Regulation of seed dormancy and germination mechanisms in a changing environment.Crossref | GoogleScholarGoogle Scholar | 33572974PubMed |

Köhler G, Hennig L, Spillane C, Pien S, Gruissem W, Grussiklaus U (2003) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes and Development 17, 1540–1553.
The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1.Crossref | GoogleScholarGoogle Scholar |

Köster T, Marondedze C, Meyer K, Staiger D (2017) RNA-binding proteins revisited – the emerging Arabidopsis MRNA interactome. Trends in Plant Science 22, 512–526.
RNA-binding proteins revisited – the emerging Arabidopsis MRNA interactome.Crossref | GoogleScholarGoogle Scholar | 28412036PubMed |

Leitner J, Retzer K, Malenica N, Bartkeviciute R, Lucyshyn D, Jäger G, et al. (2015) Meta-regulation of Arabidopsis auxin responses depends on TRNA maturation. Cell Reports 11, 516–526.
Meta-regulation of Arabidopsis auxin responses depends on TRNA maturation.Crossref | GoogleScholarGoogle Scholar | 25892242PubMed |

Lewis DR, Wu G, Ljung K, Spalding EP (2009) Auxin Transport into Cotyledons and Cotyledon Growth Depend Similarly on the ABCB19 Multidrug Resistance-like Transporter. The Plant Journal 60, 91–101.
Auxin Transport into Cotyledons and Cotyledon Growth Depend Similarly on the ABCB19 Multidrug Resistance-like Transporter.Crossref | GoogleScholarGoogle Scholar | 19508431PubMed |

Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 16731699PubMed |

Li Y, Shu Y, Peng C, Zhu L, Guo G, Li N (2012) Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism. Molecular & Cellular Proteomics 11, 272–285.
Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism.Crossref | GoogleScholarGoogle Scholar |

Liu Y, Schmidt B (2012) Long read alignment based on maximal exact match seeds. Bioinformatics 28, i318–i324.
Long read alignment based on maximal exact match seeds.Crossref | GoogleScholarGoogle Scholar | 22962447PubMed |

Liu F, Guo DD, Tu YH, Xue YR, Gao Y, Guo ML (2016) Identification of reference genes for gene expression normalization in safflower (Carthamus tinctorius). Revista Brasileira de Farmacognosia 26, 564–570.
Identification of reference genes for gene expression normalization in safflower (Carthamus tinctorius).Crossref | GoogleScholarGoogle Scholar |

Liu Y, Geyer R, van Zanten M, Carles A, Li Y, Hörold A, van Nocker S, Soppe WJJ (2011) Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. PLoS ONE 6, e22241
Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy.Crossref | GoogleScholarGoogle Scholar | 21799800PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lukowitz W, Roeder A, Parmenter D, Somerville V (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116, 109–119.
A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 14718171PubMed |

Mateo-Bonmatí E, Casanova-Sáez R, Šimura J, Ljung K (2021) Broadening the roles of UDP-glycosyltransferases in auxin homeostasis and plant development. New Phytologist 232, 642–654.
Broadening the roles of UDP-glycosyltransferases in auxin homeostasis and plant development.Crossref | GoogleScholarGoogle Scholar | 34289137PubMed |

Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marín MI, Martínez-Macías MI, Ariza RR, Roldán-Arjona T (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proceedings of the National Academy of Sciences of the United States of America 103, 6853–6858.
DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases.Crossref | GoogleScholarGoogle Scholar | 16624880PubMed |

Nakabayashi K, Bartsch M, Xiang Y, Miatton E, Pellengahr S, Yano R, et al. (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. The Plant Cell 24, 2826–2838.
The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds.Crossref | GoogleScholarGoogle Scholar | 22829147PubMed |

Née G, Kramer K, Nakabayashi K, Yuan B, Xiang Y, Miatton E, et al. (2017) DELAY Of GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nature Communications 8, 72
DELAY Of GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy.Crossref | GoogleScholarGoogle Scholar | 28706187PubMed |

Nishimura N, Tsuchiya W, Moresco JJ, Hayashi Y, Satoh K, Kaiwa N, et al. (2018) Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nature Communications 9, 2132
Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme.Crossref | GoogleScholarGoogle Scholar | 29875377PubMed |

Nonogaki H (2014) Seed dormancy and germination—emerging mechanisms and new hypotheses. Frontiers in Plant Science 5, 233
Seed dormancy and germination—emerging mechanisms and new hypotheses.Crossref | GoogleScholarGoogle Scholar | 24904627PubMed |

Penfield S, MacGregor DR (2017) Effects of environmental variation during seed production on seed dormancy and germination. Journal of Experimental Botany 68, 819–825.
Effects of environmental variation during seed production on seed dormancy and germination.Crossref | GoogleScholarGoogle Scholar | 27940467PubMed |

Pereira WJ, Bassinello PZ, Brondani C, Vianello RP (2017) An improved method for RNA extraction from common bean seeds and validation of reference genes for qPCR. Crop Breeding and Applied Biotechnology 17, 150–158.
An improved method for RNA extraction from common bean seeds and validation of reference genes for qPCR.Crossref | GoogleScholarGoogle Scholar |

Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008–1012.
Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation.Crossref | GoogleScholarGoogle Scholar | 16998468PubMed |

Qian S, Wang Y, Ma H, Zhang L (2015) Expansion and functional divergence of Jumonji C-containing histone demethylases: significance of duplications in ancestral angiosperms and vertebrates. Plant Physiology 168, 1321–1337.
Expansion and functional divergence of Jumonji C-containing histone demethylases: significance of duplications in ancestral angiosperms and vertebrates.Crossref | GoogleScholarGoogle Scholar | 26059336PubMed |

Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S (2009) Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. The Plant Journal 59, 39–51.
Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19309463PubMed |

Reimand J, Isserlin R, Voisin V, Kucera M, Tannus-Lopes C, Rostamianfar A, et al. (2019) Pathway enrichment analysis and visualization of omics data using g:Profiler, GSEA, Cytoscape and EnrichmentMap. Nature Protocols 14, 482–517.
Pathway enrichment analysis and visualization of omics data using g:Profiler, GSEA, Cytoscape and EnrichmentMap.Crossref | GoogleScholarGoogle Scholar | 30664679PubMed |

Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A, Martinho C, et al. (2013) ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein Kinase1 signaling in Arabidopsis. The Plant Cell 25, 3871–3884.
ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein Kinase1 signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24179127PubMed |

Rubio de Casas R, Willis CG, Pearse WD, Baskin CC, Baskin JM, Cavender-Bares J (2017) Global biogeography of seed dormancy is determined by seasonality and seed size: a case study in the legumes. New Phytologist 214, 1527–1536.
Global biogeography of seed dormancy is determined by seasonality and seed size: a case study in the legumes.Crossref | GoogleScholarGoogle Scholar | 28262955PubMed |

Salem MA, Li Y, Wiszniewski A, Giavalisco P (2017) Regulatory-associated protein of TOR (RAPTOR) alters the hormonal and metabolic composition of Arabidopsis seeds, controlling seed morphology, viability and germination potential. The Plant Journal 92, 525–545.
Regulatory-associated protein of TOR (RAPTOR) alters the hormonal and metabolic composition of Arabidopsis seeds, controlling seed morphology, viability and germination potential.Crossref | GoogleScholarGoogle Scholar | 28845535PubMed |

Schoft VK, Chumak N, Choi Y, Hannon M, Garcia-Aguilar M, Machlicova A, et al. (2011) Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proceedings of the National Academy of Sciences of the United States of America 108, 8042–8047.
Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte.Crossref | GoogleScholarGoogle Scholar | 21518889PubMed |

Shu K, Liu X-d, Xie Q, He Z-h (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Molecular Plant 9, 34–45.
Two faces of one seed: hormonal regulation of dormancy and germination.Crossref | GoogleScholarGoogle Scholar | 26343970PubMed |

Singh M, Singh J (2012) Seed development-related expression of ARGONAUTE4_9 class of genes in barley: possible role in seed dormancy. Euphytica 188, 123–129.
Seed development-related expression of ARGONAUTE4_9 class of genes in barley: possible role in seed dormancy.Crossref | GoogleScholarGoogle Scholar |

Sohindji FS, Sogbohossou DEO, Zohoungbogbo HPF, Houdegbe CA, Achigan-Dako EG (2020) Understanding molecular mechanisms of seed dormancy for improved germination in traditional leafy vegetables: an overview. Agronomy 10, 57
Understanding molecular mechanisms of seed dormancy for improved germination in traditional leafy vegetables: an overview.Crossref | GoogleScholarGoogle Scholar |

Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa PM, et al. (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447, 735–738.
Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination.Crossref | GoogleScholarGoogle Scholar | 17554311PubMed |

Sugliani M, Brambilla V, Clerkx EJM, Koornneef M, Soppe WJJ (2010) The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in Arabidopsis. The Plant Cell 22, 1936–1946.
The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20525852PubMed |

Tamada Y, Yun JY, Woo Sc, Amasino RM (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. The Plant Cell 21, 3257–3269.
ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C.Crossref | GoogleScholarGoogle Scholar | 19855050PubMed |

Vaishnav K, George LB, Highland HN (2015) Antitumour activity of Xanthium strumarium L. on human cervical cancer HeLa cells. Journal of Cancer and Tumor International 2, 1–13.
Antitumour activity of Xanthium strumarium L. on human cervical cancer HeLa cells.Crossref | GoogleScholarGoogle Scholar |

Vaistij FE, Gan Y, Penfield S, Gilday AD, Dave A, He Z, et al. (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proceedings of the National Academy of Sciences of the United States of America 110, 10866–10871.
Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA.Crossref | GoogleScholarGoogle Scholar | 23754415PubMed |

Vlieghe K, Boudolf V, Beemster GTS, Maes S, Magyar Z, Atanassova A, et al. (2005) The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis Thaliana. Current Biology 15, 59–63.
The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis Thaliana.Crossref | GoogleScholarGoogle Scholar | 15649366PubMed |

Wang Z, Cao H, Sun Y, Li X, Chen F, Carles A, et al. (2013) Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid–ethylene antagonism mediated by histone deacetylation. The Plant Cell 25, 149–166.
Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid–ethylene antagonism mediated by histone deacetylation.Crossref | GoogleScholarGoogle Scholar | 23371947PubMed |

Wei L, Miao H, Zhao R, Han X, Zhang T, Zhang H (2013) Identification and testing of reference genes for sesame gene expression analysis by quantitative real-time PCR. Planta 237, 873–889.
Identification and testing of reference genes for sesame gene expression analysis by quantitative real-time PCR.Crossref | GoogleScholarGoogle Scholar | 23229061PubMed |

Weiste C, Dröge-Laser W (2014) The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nature Communications 5, 3883
The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery.Crossref | GoogleScholarGoogle Scholar | 24861440PubMed |

Xu F, Kuo T, Rosli Y, Liu MS, Wu L, Chen L-FO, et al. (2018) Trithorax group proteins act together with a polycomb group protein to maintain chromatin integrity for epigenetic silencing during seed germination in Arabidopsis. Molecular Plant 11, 659–677.
Trithorax group proteins act together with a polycomb group protein to maintain chromatin integrity for epigenetic silencing during seed germination in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29428247PubMed |

Yu Z, Lin J, Li QQ (2019) Transcriptome analyses of FY mutants reveal its role in mRNA alternative polyadenylation. The Plant Cell 31, 2332–2352.
Transcriptome analyses of FY mutants reveal its role in mRNA alternative polyadenylation.Crossref | GoogleScholarGoogle Scholar | 31427469PubMed |

Zhan X, Qian B, Cao F, Wu W, Yang L, Guan Q, et al. (2015) An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses. Nature Communications 6, 8139
An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses.Crossref | GoogleScholarGoogle Scholar | 26404089PubMed |

Zheng J, Chen F, Wang Z, Cao H, Li X, Deng X, et al. (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytologist 193, 605–616.
A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy.Crossref | GoogleScholarGoogle Scholar | 22122546PubMed |

Zhou W, Wang S, Yang L, Sun Y, Zhang Q, Li B, et al. (2019) Reference genes for QRT-PCR normalisation in different tissues, developmental stages, and stress conditions of hypericum perforatum. PeerJ 7, e7133
Reference genes for QRT-PCR normalisation in different tissues, developmental stages, and stress conditions of hypericum perforatum.Crossref | GoogleScholarGoogle Scholar | 31259099PubMed |