The entire process of embryo development is under the tight control of various transcription factors. Together with other proteins, they act in a combinatorial manner and control distinct events during embryo development. Seed development is a complex process that proceeds through sequences of events regulated by the interplay of various genes, prominent among them being the transcription factors (TFs). The members of WOX, HD-ZIP III, ARF, and CUC families have a preferential role in embryonic patterning. While WOX TFs are required for initiating body axis, HD-ZIP III TFs and CUCs establish bilateral symmetry and SAM. And ARF5 performs a major role during embryonic root, ground tissue, and vasculature development. TFs such as LEC1, ABI3, FUS3, and LEC2 (LAFL) are considered the master regulators of seed maturation. Furthermore, several new TFs involved in seed storage reserves and dormancy have been identified in the last few years. Their association with those master regulators has been established in the model plant Arabidopsis. Also, using chromatin immunoprecipitation (ChIP) assay coupled with transcriptomics, genome-wide target genes of these master regulators have recently been proposed. Many seed-specific genes, including those encoding oleosins and albumins, have appeared as the direct target of LAFL. Also, several other TFs act downstream of LAFL TFs and perform their function during maturation. In this review, the function of different TFs in different phases of early embryogenesis and maturation is discussed in detail, including information about their genetic and molecular interactors and target genes. Such knowledge can further be leveraged to understand and manipulate the regulatory mechanisms involved in seed development. In addition, the genomics approaches and their utilization to identify TFs aiming to study embryo development are discussed.

Mendel Centre for Genomics and Proteomics of Plants Systems CEITEC MU Central European Institute of Technology Masaryk University Brno Czech Republic

Zobrazit více v PubMed

Abe M, Katsumata H, Komeda Y, Takahashi T. Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development (Cambridge, England) 2003;130(4):635–643. doi: 10.1242/dev.00292. PubMed DOI

Agarwal P, Kapoor S, Tyagi AK. Transcription factors regulating the progression of monocot and dicot seed development. BioEssays . 2011;33(3):189–202. doi: 10.1002/bies.201000107. PubMed DOI

Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell. 2004;119(1):109–120. doi: 10.1016/j.cell.2004.09.018. PubMed DOI

Aida M, Ishida T, Tasaka M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development (Cambridge, England) 1999;126(8):1563–1570. doi: 10.1242/dev.126.8.1563. PubMed DOI

Ali F, Qanmber G, Li F, Wang Z. Updated role of ABA in seed maturation, dormancy, and germination. J Adv Res. 2021 doi: 10.1016/j.jare.2021.03.011. PubMed DOI PMC

Alonso R, Oñate-Sánchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Dröge-Laser W. A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell. 2009;21(6):1747–1761. doi: 10.1105/tpc.108.062968. PubMed DOI PMC

Andrilenas KK, Penvose A, Siggers T. Using protein-binding microarrays to study transcription factor specificity: homologs, isoforms and complexes. Brief Funct Genomics. 2015;14(1):17–29. doi: 10.1093/bfgp/elu046. PubMed DOI PMC

Baroux C, Grossniklaus U. Seeds-An evolutionary innovation underlying reproductive success in flowering plants. Curr Top Dev Biol. 2019;131:605–642. doi: 10.1016/bs.ctdb.2018.11.017. PubMed DOI

Batista RA, Moreno-Romero J, Qiu Y, van Boven J, Santos-González J, Figueiredo DD, Köhler C (2019) The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons. eLife 8:e50541. doi:10.7554/eLife.50541 PubMed PMC

Baud S, Boutin J-P, Miquel M, Lepiniec L, Rochat C. An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem. 2002;40(2):151–160. doi: 10.1016/S0981-9428(01)01350-X. DOI

Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L. Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. Arabidopsis Book. 2008;6:e0113–e0113. doi: 10.1199/tab.0113. PubMed DOI PMC

Baud S, Kelemen Z, Thévenin J. Deciphering the molecular mechanisms underpinning the transcriptional control of gene expression by master transcriptional regulators in Arabidopsis seed. Plant Physiol. 2016;171(2):1099–1112. doi: 10.1104/pp.16.00034. PubMed DOI PMC

Baud S, Mendoza MS, To A, Harscoët E, Lepiniec L, Dubreucq B. WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007;50(5):825–838. doi: 10.1111/j.1365-313X.2007.03092.x. PubMed DOI

Bäumlein H, Miséra S, Luerssen H, Kölle K, Horstmann C, Wobus U, Müller A. The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. Plant J. 1994;6:379–387. doi: 10.1046/j.1365-313X.1994.06030379.x. DOI

Berleth T, Jurgens G. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development (Cambridge, England) 1993;118(2):575–587. doi: 10.1242/dev.118.2.575. DOI

Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S, Mitchell A, Nuka G, Paysan-Lafosse T, Qureshi M, Raj S, Richardson L, Salazar GA, Williams L, Bork P, Bridge A, Gough J, Haft DH, Letunic I, Marchler-Bauer A, Mi H, Natale DA, Necci M, Orengo CA, Pandurangan AP, Rivoire C, Sigrist CJA, Sillitoe I, Thanki N, Thomas PD, Tosatto SCE, Wu CH, Bateman A, Finn RD. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res. 2021;49(D1):D344–D354. doi: 10.1093/nar/gkaa977. PubMed DOI PMC

Borghi L. Inducible gene expression systems for plants. Methods Mol Biol (Clifton, NJ) 2010;655:65–75. doi: 10.1007/978-1-60761-765-5_5. PubMed DOI

Boulard C, Fatihi A, Lepiniec L, Dubreucq B. Regulation and evolution of the interaction of the seed B3 transcription factors with NF-Y subunits. Biochim Biophys Acta. 2017;1860(10):1069–1078. doi: 10.1016/j.bbagrm.2017.08.008. PubMed DOI

Braybrook SA, Harada JJ. LECs go crazy in embryo development. Trends Plant Sci. 2008;13(12):624–630. doi: 10.1016/j.tplants.2008.09.008. PubMed DOI

Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, Fischer RL, Goldberg RB, Harada JJ. Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA. 2006;103(9):3468–3473. doi: 10.1073/pnas.0511331103. PubMed DOI PMC

Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell. 2008;14(6):867–876. doi: 10.1016/j.devcel.2008.03.008. PubMed DOI

Brown RC, Lemmon BE, Nguyen H, Olsen O-A. Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod. 1999;12(1):32–42. doi: 10.1007/s004970050169. DOI

Bryant FM, Hughes D. Basic LEUCINE ZIPPER TRANSCRIPTION FACTOR67 transactivates DELAY OF GERMINATION1 to establish primary seed dormancy in Arabidopsis. Plant Cell. 2019;31(6):1276–1288. doi: 10.1105/tpc.18.00892. PubMed DOI PMC

Buijs G. A perspective on secondary seed dormancy in Arabidopsis thaliana. Plants (Basel, Switzerland) 2020;9(6):749. doi: 10.3390/plants9060749. PubMed DOI PMC

Capron A, Chatfield S, Provart N, Berleth T. Embryogenesis: pattern formation from a single cell. Arabidopsis Book. 2009;7:e0126–e0126. doi: 10.1199/tab.0126. PubMed DOI PMC

Carrillo-Barral N, Rodríguez-Gacio MDC, Matilla AJ. Delay of Germination-1 (DOG1): a key to understanding seed dormancy. Plants (Basel, Switzerland) 2020;9(4):480. doi: 10.3390/plants9040480. PubMed DOI PMC

Chandler JW, Cole M, Flier A, Grewe B, Werr W. The AP2 transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development (Cambridge, England) 2007;134(9):1653–1662. doi: 10.1242/dev.001016. PubMed DOI

Chen M, Xuan L, Wang Z, Zhou L, Li Z, Du X, Ali E, Zhang G, Jiang L. TRANSPARENT TESTA8 inhibits seed fatty acid accumulation by targeting several seed development regulators in Arabidopsis. Plant Physiol. 2014;165(2):905–916. doi: 10.1104/pp.114.235507. PubMed DOI PMC

Chen M, Zhang B, Li C, Kulaveerasingam H, Chew FT, Yu H. TRANSPARENT TESTA GLABRA1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol. 2015;169(1):391–402. doi: 10.1104/pp.15.00943. PubMed DOI PMC

Chen N, Veerappan V, Abdelmageed H, Kang M, Allen RD. HSI2/VAL1 silences AGL15 to regulate the developmental transition from seed maturation to vegetative growth in Arabidopsis. Plant Cell. 2018;30(3):600–619. doi: 10.1105/tpc.17.00655. PubMed DOI PMC

Cole M, Chandler J, Weijers D, Jacobs B, Comelli P, Werr W. DORNRÖSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development (Cambridge, England) 2009;136(10):1643–1651. doi: 10.1242/dev.032177. PubMed DOI

Crawford BCW, Sewell J, Golembeski G, Roshan C, Long Jeff A, Yanofsky Martin F. Genetic control of distal stem cell fate within root and embryonic meristems. Science. 2015;347(6222):655–659. doi: 10.1126/science.aaa0196. PubMed DOI

De Rybel B, Adibi M, Breda Alice S, Wendrich Jos R, Smit Margot E, Novák O, Yamaguchi N, Yoshida S, Van Isterdael G, Palovaara J, Nijsse B, Boekschoten Mark V, Hooiveld G, Beeckman T, Wagner D, Ljung K, Fleck C, Weijers D. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science. 2014;345(6197):1255215. doi: 10.1126/science.1255215. PubMed DOI

De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith Richard S, Borst Jan W, Weijers D. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell. 2013;24(4):426–437. doi: 10.1016/j.devcel.2012.12.013. PubMed DOI

Dekkers BJ, He H, Hanson J, Willems LA, Jamar DC, Cueff G, Rajjou L, Hilhorst HW, Bentsink L. The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. Plant J. 2016;85(4):451–465. doi: 10.1111/tpj.13118. PubMed DOI

Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JGB, McCourt P, Samuel MA. ABI3 controls embryo degreening through Mendel's locus. Proc Natl Acad Sci USA. 2013;110(40):E3888. doi: 10.1073/pnas.1308114110. PubMed DOI PMC

Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ. WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J. 2014;79(5):810–823. doi: 10.1111/tpj.12597. PubMed DOI

Dolfini D, Gatta R, Mantovani R. NF-Y and the transcriptional activation of CCAAT promoters. Crit Rev Biochem Mol Biol. 2012;47(1):29–49. doi: 10.3109/10409238.2011.628970. PubMed DOI

Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL. Radial patterning of Arabidopsis shoots by Class III HD-ZIP and KANADI genes. Curr Biol. 2003;13(20):1768–1774. doi: 10.1016/j.cub.2003.09.035. PubMed DOI

Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL. Asymmetric leaf development and blade expansion in Arabidopsisare mediated by KANADI and YABBY activities. Development (Cambridge, England) 2004;131(12):2997–3006. doi: 10.1242/dev.01186. PubMed DOI

Finkelstein R, Reeves W, Ariizumi T, Steber C. Molecular aspects of seed dormancy. Annu Rev Plant Biol. 2008;59:387–415. doi: 10.1146/annurev.arplant.59.032607.092740. PubMed DOI

Finkelstein RR. Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J. 1994;5(6):765–771. doi: 10.1046/j.1365-313X.1994.5060765.x. DOI

Floyd SK, Bowman JL. Ancient microRNA target sequences in plants. Nature. 2004;428(6982):485–486. doi: 10.1038/428485a. PubMed DOI

Francoz E, Lepiniec L, North HM. Seed coats as an alternative molecular factory: thinking outside the box. Plant Reprod. 2018;31(3):327–342. doi: 10.1007/s00497-018-0345-2. PubMed DOI

Frandsen GI, Mundy J, Tzen JTC. Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant. 2001;112(3):301–307. doi: 10.1034/j.1399-3054.2001.1120301.x. PubMed DOI

Gacek K, Bartkowiak-Broda I, Batley J. Genetic and molecular regulation of seed storage proteins (SSPs) to improve protein nutritional value of oilseed rape (Brassica napus L.) Seeds. Front Plant Sci. 2018;9:890. doi: 10.3389/fpls.2018.00890. PubMed DOI PMC

Gao C, Qi S, Liu K, Li D, Jin C, Li Z, Huang G, Hai J, Zhang M, Chen M. MYC2, MYC3, and MYC4 function redundantly in seed storage protein accumulation in Arabidopsis. Plant Physiology and Biochemistry : PPB. 2016;108:63–70. doi: 10.1016/j.plaphy.2016.07.004. PubMed DOI

Goldberg RB, de Paiva G, Yadegari R. Plant Embryogenesis: Zygote to Seed. Science. 1994;266(5185):605–614. doi: 10.1126/science.266.5185.605. PubMed DOI

Golz JF, Allen PJ, Li SF, Parish RW, Jayawardana NU, Bacic A, Doblin MS. Layers of regulation – Insights into the role of transcription factors controlling mucilage production in the Arabidopsis seed coat. Plant Sci. 2018;272:179–192. doi: 10.1016/j.plantsci.2018.04.021. PubMed DOI

González-Morales SI, Chávez-Montes RA, Hayano-Kanashiro C, Alejo-Jacuinde G, Rico-Cambron TY, de Folter S, Herrera-Estrella L. Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2016;113(35):E5232–5241. doi: 10.1073/pnas.1610985113. PubMed DOI PMC

Gu W, Yu D, Guan Y, Wang H, Qin T, Sun P, Hu Y, Wei J, Zheng H. The dynamic transcriptome of waxy maize (Zea mays L. sinensis Kulesh) during seed development. Genes Genomics. 2020;42(9):997–1010. doi: 10.1007/s13258-020-00967-z. PubMed DOI

Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development (Cambridge, England) 2004;131(3):657–668. doi: 10.1242/dev.00963. PubMed DOI

Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 2002;16(13):1610–1615. doi: 10.1101/gad.229402. PubMed DOI PMC

Hamann T, Mayer U, Jürgens G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development (Cambridge, England) 1999;126(7):1387–1395. doi: 10.1242/dev.126.7.1387. PubMed DOI

Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000;101(5):555–567. doi: 10.1016/s0092-8674(00)80865-x. PubMed DOI

Hofmann F, Schon MA, Nodine MD. The embryonic transcriptome of Arabidopsis thaliana. Plant Reprod. 2019;32(1):77–91. doi: 10.1007/s00497-018-00357-2. PubMed DOI

Hu S, Xie Z, Onishi A, Yu X, Jiang L, Lin J, Rho H-s, Woodard C, Wang H, Jeong J-S, Long S, He X, Wade H, Blackshaw S, Qian J, Zhu H. Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell. 2009;139(3):610–622. doi: 10.1016/j.cell.2009.08.037. PubMed DOI PMC

Hung Y-H, Slotkin RK. The initiation of RNA interference (RNAi) in plants. Curr Opin Plant Biol. 2021;61:102014. doi: 10.1016/j.pbi.2021.102014. PubMed DOI

Iida H, Yoshida A, Takada S. ATML1 activity is restricted to the outermost cells of the embryo through post-transcriptional repressions. Development (Cambridge, England) 2019;146(4):dev169300. doi: 10.1242/dev.169300. PubMed DOI

Izhaki A, Bowman JL. KANADI and Class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell. 2007;19(2):495–508. doi: 10.1105/tpc.106.047472. PubMed DOI PMC

Jeong HJ, Choi JY, Shin HY, Bae JM, Shin JS. Seed-specific expression of seven Arabidopsis promoters. Gene. 2014;553(1):17–23. doi: 10.1016/j.gene.2014.09.051. PubMed DOI

Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017;45(D1):D1040–D1045. doi: 10.1093/nar/gkw982. PubMed DOI PMC

Jo L, Pelletier JM, Harada JJ. Central role of the LEAFY COTYLEDON1 transcription factor in seed development. J Integr Plant Biol. 2019;61(5):564–580. doi: 10.1111/jipb.12806. PubMed DOI

Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T. Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol. 2005;46(2):300–311. doi: 10.1093/pcp/pci031. PubMed DOI

Kao P, Schon MA, Mosiolek M, Enugutti B, Nodine MD. Gene expression variation in Arabidopsis embryos at single-nucleus resolution. Development (Cambridge, England) 2021;148(13):dev199589. doi: 10.1242/dev.199589. PubMed DOI PMC

Keith K, Kraml M, Dengler NG, McCourt P. fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell. 1994;6(5):589–600. doi: 10.1105/tpc.6.5.589. PubMed DOI PMC

Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS. KANADI regulates organ polarity in Arabidopsis. Nature. 2001;411(6838):706–709. doi: 10.1038/35079629. PubMed DOI

Kijak H, Ratajczak E. What Do We Know About the Genetic Basis of Seed Desiccation Tolerance and Longevity? International Journal of Molecular Sciences. 2020;21(10):3612. doi: 10.3390/ijms21103612. PubMed DOI PMC

Kodama M, Brinch-Pedersen H, Sharma S, Holme IB, Joernsgaard B, Dzhanfezova T, Amby DB, Vieira FG, Liu S, Gilbert MTP. Identification of transcription factor genes involved in anthocyanin biosynthesis in carrot (Daucus carota L.) using RNA-Seq. BMC Genomics. 2018;19(1):811. doi: 10.1186/s12864-018-5135-6. PubMed DOI PMC

Kong Q, Singh SK, Mantyla JJ. TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR4 Interacts with WRINKLED1 to mediate seed oil biosynthesis. Plant Physiol. 2020;184(2):658–665. doi: 10.1104/pp.20.00547. PubMed DOI PMC

Kong Q, Yuan L, Ma W. WRINKLED1, a "Master Regulator" in transcriptional control of plant oil biosynthesis. Plant (Basel) 2019;8(7):238. doi: 10.3390/plants8070238. PubMed DOI PMC

Kroj T, Savino G, Valon C, Giraudat J, Parcy F. Regulation of storage protein gene expression in Arabidopsis. Development (Cambridge, England) 2003;130(24):6065–6073. doi: 10.1242/dev.00814. PubMed DOI

Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Díaz I, Carbonero P, Vicente-Carbajosa J. Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem. 2003;278(23):21003–21011. doi: 10.1074/jbc.M210538200. PubMed DOI

Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA. 2010;107(18):8063. doi: 10.1073/pnas.1003530107. PubMed DOI PMC

Lepiniec L, Devic M, Roscoe TJ, Bouyer D, Zhou DX, Boulard C, Baud S, Dubreucq B. Molecular and epigenetic regulations and functions of the LAFL transcriptional regulators that control seed development. Plant Reprod. 2018;31(3):291–307. doi: 10.1007/s00497-018-0337-2. PubMed DOI

Leprince O, Pellizzaro A, Berriri S, Buitink J. Late seed maturation: drying without dying. J Exp Bot. 2017;68(4):827–841. doi: 10.1093/jxb/erw363. PubMed DOI

Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 2021;49(D1):D458–D460. doi: 10.1093/nar/gkaa937. PubMed DOI PMC

Leviczky T, Molnár E, Papdi C, Őszi E, Horváth GV, Vizler C, Nagy V, Pauk J, Bögre L, Magyar Z. E2FA and E2FB transcription factors coordinate cell proliferation with seed maturation. Development. 2019;146(22):dev179333. doi: 10.1242/dev.179333. PubMed DOI PMC

Li D, Jin C, Duan S, Zhu Y, Qi S, Liu K, Gao C, Ma H, Zhang M, Liao Y, Chen M. MYB89 transcription factor represses seed oil accumulation. Plant Physiol. 2017;173(2):1211–1225. doi: 10.1104/pp.16.01634. PubMed DOI PMC

Li J, Berger F. Endosperm: food for humankind and fodder for scientific discoveries. New Phytol. 2012;195(2):290–305. doi: 10.1111/j.1469-8137.2012.04182.x. PubMed DOI

Li X, Chen T, Li Y, Wang Z, Cao H, Chen F, Li Y, Soppe WJJ, Li W, Liu Y. ETR1/RDO3 regulates seed dormancy by relieving the inhibitory effect of the ERF12-TPL complex on DELAY OF GERMINATION1 expression. Plant Cell. 2019;31(4):832–847. doi: 10.1105/tpc.18.00449. PubMed DOI PMC

Liao C-Y, Weijers D. A toolkit for studying cellular reorganization during early embryogenesis in Arabidopsis thaliana. Plant J. 2018;93(6):963–976. doi: 10.1111/tpj.13841. PubMed DOI PMC

Lie C, Kelsom C, Wu X. WOX2 and STIMPY-LIKE/WOX8 promote cotyledon boundary formation in Arabidopsis. Plant J . 2012;72(4):674–682. doi: 10.1111/j.1365-313X.2012.05113.x. PubMed DOI

Liu X, Wu S, Xu J, Sui C, Wei J. Application of CRISPR/Cas9 in plant biology. Acta Pharm Sin B. 2017;7(3):292–302. doi: 10.1016/j.apsb.2017.01.002. PubMed DOI PMC

Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang H-Q, Luan S, Li J, He Z-H. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA. 2013;110(38):15485. doi: 10.1073/pnas.1304651110. PubMed DOI PMC

Lotan T, Ohto M-a, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell. 1998;93(7):1195–1205. doi: 10.1016/S0092-8674(00)81463-4. PubMed DOI

Lu P, Porat R, Nadeau JA, O'Neill SD. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell. 1996;8(12):2155–2168. doi: 10.1105/tpc.8.12.2155. PubMed DOI PMC

MacGregor DR, Zhang N. ICE1 and ZOU determine the depth of primary seed dormancy in Arabidopsis independently of their role in endosperm development. Plant J. 2019;98(2):277–290. doi: 10.1111/tpj.14211. PubMed DOI PMC

Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K. An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 2009;60(3):476–487. doi: 10.1111/j.1365-313X.2009.03967.x. PubMed DOI

Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J. 2004;23(16):3356–3364. doi: 10.1038/sj.emboj.7600340. PubMed DOI PMC

Mansfield SG, Briarty LG. Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot. 1991;69(3):461–476. doi: 10.1139/b91-063. DOI

Mathew IE, Priyadarshini R, Mahto A, Jaiswal P, Parida SK, Agarwal P. SUPER STARCHY1/ONAC025 participates in rice grain filling. Plant Direct. 2020;4(9):e00249. doi: 10.1002/pld3.249. PubMed DOI PMC

McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature. 2001;411(6838):709–713. doi: 10.1038/35079635. PubMed DOI

Meinke DW, Franzmann LH, Nickle TC, Yeung EC. Leafy cotyledon mutants of Arabidopsis. Plant Cell. 1994;6(8):1049–1064. doi: 10.1105/tpc.6.8.1049. PubMed DOI PMC

Mendes A, Kelly AA, van Erp H, Shaw E, Powers SJ, Kurup S, Eastmond PJ. bZIP67 regulates the omega-3 fatty acid content of Arabidopsis seed oil by activating FATTY ACID DESATURASE3. Plant Cell. 2013;25(8):3104–3116. doi: 10.1105/tpc.113.116343. PubMed DOI PMC

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar Gustavo A, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A. Pfam: The protein families database in 2021. Nucleic Acids Res. 2021;49(D1):D412–D419. doi: 10.1093/nar/gkaa913. PubMed DOI PMC

Möller BK, ten Hove CA, Xiang D, Williams N, López LG, Yoshida S, Smit M, Datla R, Weijers D. Auxin response cell-autonomously controls ground tissue initiation in the early <em>Arabidopsis</em> embryo. Proc Natl Acad Sci USA. 2017;114(12):E2533. doi: 10.1073/pnas.1616493114. PubMed DOI PMC

Mönke G, Altschmied L, Tewes A, Reidt W, Mock H-P, Bäumlein H, Conrad U. Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta. 2004;219(1):158–166. doi: 10.1007/s00425-004-1206-9. PubMed DOI

Mönke G, Seifert M, Keilwagen J, Mohr M, Grosse I, Hähnel U, Junker A, Weisshaar B, Conrad U, Bäumlein H, Altschmied L. Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res. 2012;40(17):8240–8254. doi: 10.1093/nar/gks594. PubMed DOI PMC

Mu J, Tan H, Zheng Q, Fu F, Liang Y, Zhang J, Yang X, Wang T, Chong K, Wang X-J, Zuo J. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 2008;148(2):1042–1054. doi: 10.1104/pp.108.126342. PubMed DOI PMC

Nakajima K, Sena G, Nawy T, Benfey PN. Intercellular movement of the putative transcription factor SHR in root patterning. Nature. 2001;413(6853):307–311. doi: 10.1038/35095061. PubMed DOI

Nambara E, Nambara E, McCourt P, Naito S. A regulatory role for the ABI3 gene in the establishment of embryo maturation in Arabidopsis thaliana. Development (Cambridge, England) 1995;121(3):629–636. doi: 10.1242/dev.121.3.629. DOI

Née G, Xiang Y, Soppe WJJ. The release of dormancy, a wake-up call for seeds to germinate. Curr Opin Plant Biol. 2017;35:8–14. doi: 10.1016/j.pbi.2016.09.002. PubMed DOI

Nonogaki H. Seed germination and dormancy: The classic story, new puzzles, and evolution. J Integr Plant Biol. 2019;61(5):541–563. doi: 10.1111/jipb.12762. PubMed DOI

O'Neill JP, Colon KT, Jenik PD. The onset of embryo maturation in Arabidopsis is determined by its developmental stage and does not depend on endosperm cellularization. Plant J. 2019;99(2):286–301. doi: 10.1111/tpj.14324. PubMed DOI PMC

Ogawa E, Yamada Y, Sezaki N, Kosaka S, Kondo H, Kamata N, Abe M, Komeda Y, Takahashi T. ATML1 and PDF2 play a redundant and essential role in Arabidopsis embryo development. Plant Cell Physiol. 2015;56(6):1183–1192. doi: 10.1093/pcp/pcv045. PubMed DOI

Palovaara J, Saiga S, Weijers D. Transcriptomics approaches in the early Arabidopsis embryo. Trends Plant Sci. 2013;18(9):514–521. doi: 10.1016/j.tplants.2013.04.011. PubMed DOI

Parcy F, Valon C, Kohara A, Miséra S, Giraudat J. The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell. 1997;9(8):1265–1277. doi: 10.1105/tpc.9.8.1265. PubMed DOI PMC

Pelletier JM, Kwong RW, Park S, Le BH, Baden R, Cagliari A, Hashimoto M, Munoz MD, Fischer RL, Goldberg RB, Harada JJ. LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc Natl Acad Sci USA. 2017;114(32):E6710. doi: 10.1073/pnas.1707957114. PubMed DOI PMC

Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J. 2015;13(4):578–589. doi: 10.1111/pbi.12284. PubMed DOI

Pradhan S, Bandhiwal N, Shah N, Kant C, Gaur R, Bhatia S. Global transcriptome analysis of developing chickpea (Cicer arietinum L.) seeds. Front Plant Sci. 2014;5:698–698. doi: 10.3389/fpls.2014.00698. PubMed DOI PMC

Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell. 2005;17(1):61–76. doi: 10.1105/tpc.104.026161. PubMed DOI PMC

Reece-Hoyes JS, Marian Walhout AJ. Yeast one-hybrid assays: a historical and technical perspective. Methods (San Diego, Calif) 2012;57(4):441–447. doi: 10.1016/j.ymeth.2012.07.027. PubMed DOI PMC

Reidt W, Wohlfarth T, Ellerström M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H. Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J. 2000;21(5):401–408. doi: 10.1046/j.1365-313x.2000.00686.x. PubMed DOI

Ren Y, Huang Z, Jiang H, Wang Z, Wu F, Xiong Y, Yao J. A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling. J Exp Bot. 2021;72(8):2947–2964. doi: 10.1093/jxb/erab027. PubMed DOI

Roscoe TT, Guilleminot J, Bessoule J-J, Berger F, Devic M. Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol. 2015;56(6):1215–1228. doi: 10.1093/pcp/pcv049. PubMed DOI

Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 2008;54(4):608–620. doi: 10.1111/j.1365-313X.2008.03461.x. PubMed DOI

Sasnauskas G, Manakova E, Lapėnas K, Kauneckaitė K, Siksnys V. DNA recognition by Arabidopsis transcription factors ABI3 and NGA1. FEBS J. 2018;285(21):4041–4059. doi: 10.1111/febs.14649. PubMed DOI

Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010;464(7290):913–916. doi: 10.1038/nature08836. PubMed DOI

Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q. ABI4 Regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet. 2013;9(6):e1003577. doi: 10.1371/journal.pgen.1003577. PubMed DOI PMC

Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development (Cambridge, England) 1999;126(18):4117–4128. doi: 10.1242/dev.126.18.4117. PubMed DOI

Smit ME, Llavata-Peris CI, Roosjen M, van Beijnum H, Novikova D, Levitsky V, Sevilem I, Roszak P, Slane D, Jürgens G, Mironova V, Brady SM, Weijers D. Specification and regulation of vascular tissue identity in the Arabidopsis embryo. Development (Cambridge, England) 2020;147(8):dev186130. doi: 10.1242/dev.186130. PubMed DOI

Smith ZR, Long JA. Control of Arabidopsis apical–basal embryo polarity by antagonistic transcription factors. Nature. 2010;464(7287):423–426. doi: 10.1038/nature08843. PubMed DOI PMC

Song J, Xie X, Chen C, Shu J, Thapa RK, Nguyen V, Bian S, Kohalmi SE, Marsolais F, Zou J, Cui Y. LEAFY COTYLEDON1 expression in the endosperm enables embryo maturation in Arabidopsis. Nat Commun. 2021;12(1):3963. doi: 10.1038/s41467-021-24234-1. PubMed DOI PMC

Spitz F, Furlong EEM. Transcription factors: from enhancer binding to developmental control. Nat Rev Genet. 2012;13(9):613–626. doi: 10.1038/nrg3207. PubMed DOI

Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh TF, Fischer RL, Goldberg RB, Harada JJ. Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc Natl Acad Sci USA. 2008;105(8):3151–3156. doi: 10.1073/pnas.0712364105. PubMed DOI PMC

Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA. 2001;98(20):11806–11811. doi: 10.1073/pnas.201413498. PubMed DOI PMC

Suzuki M, Wang HHY, McCarty DR. Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes. Plant Physiol. 2007;143(2):902–911. doi: 10.1104/pp.106.092320. PubMed DOI PMC

Tacheny A, Dieu M, Arnould T, Renard P. Mass spectrometry-based identification of proteins interacting with nucleic acids. J Proteomics. 2013;94:89–109. doi: 10.1016/j.jprot.2013.09.011. PubMed DOI

Takada S, Hibara K, Ishida T, Tasaka M. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development (Cambridge, England) 2001;128(7):1127–1135. doi: 10.1242/dev.128.7.1127. PubMed DOI

Takada S, Jürgens G. Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development (Cambridge, England) 2007;134(6):1141–1150. doi: 10.1242/dev.02803. PubMed DOI

Tian R, Wang F, Zheng Q, Niza V, Downie AB. Direct and indirect targets of the arabidopsis seed transcription factor ABSCISIC ACID INSENSITIVE3. Plant J. 2020;103(5):1679–1694. doi: 10.1111/tpj.14854. PubMed DOI

To A, Valon C, Savino G, Guilleminot J, Devic M, Jrm G, Fo P. A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell. 2006;18(7):1642–1651. doi: 10.1105/tpc.105.039925. PubMed DOI PMC

Tsukagoshi H, Morikami A, Nakamura K. Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings. Proc Natl Acad Sci USA. 2007;104(7):2543–2547. doi: 10.1073/pnas.0607940104. PubMed DOI PMC

Turchi L, Carabelli M, Ruzza V, Possenti M, Sassi M, Peñalosa A, Sessa G, Salvi S, Forte V, Morelli G, Ruberti I. Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development (Cambridge, England) 2013;140(10):2118–2129. doi: 10.1242/dev.092833. PubMed DOI

Ueda M, Zhang Z, Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell. 2011;20(2):264–270. doi: 10.1016/j.devcel.2011.01.009. PubMed DOI

Vaistij FE, Gan Y, Penfield S, Gilday AD, Dave A, He Z, Josse EM, Choi G, Halliday KJ, Graham IA. Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proc Natl Acad Sci USA. 2013;110(26):10866–10871. doi: 10.1073/pnas.1301647110. PubMed DOI PMC

Veerappan V, Wang J, Kang M, Lee J, Tang Y, Jha AK, Shi H, Palanivelu R, Allen RD. A novel HSI2 mutation in Arabidopsis affects the PHD-like domain and leads to derepression of seed-specific gene expression. Planta. 2012;236(1):1–17. doi: 10.1007/s00425-012-1630-1. PubMed DOI

Verma S, Attuluri VPS, Robert HS. An essential function for auxin in embryo development. Cold Spring Harbor Perspect Biology. 2021 doi: 10.1101/cshperspect.a039966. PubMed DOI PMC

Verma S, Bhatia S. Analysis of genes encoding seed storage proteins (SSPs) in chickpea (Cicer arietinum L.) reveals co-expressing transcription factors and a seed-specific promoter. Funct Integr Genomics. 2019;19(3):373–390. doi: 10.1007/s10142-018-0650-8. PubMed DOI

Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell. 2003;15(7):1563–1577. doi: 10.1105/tpc.012203. PubMed DOI PMC

Wang F, Perry SE. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 2013;161(3):1251–1264. doi: 10.1104/pp.112.212282. PubMed DOI PMC

West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ. LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell. 1994;6(12):1731–1745. doi: 10.1105/tpc.6.12.1731. PubMed DOI PMC

Wu Q, Bai X, Wu X, Xiang D, Wan Y, Luo Y, Shi X, Li Q, Zhao J, Qin P, Yang X, Zhao G. Transcriptome profiling identifies transcription factors and key homologs involved in seed dormancy and germination regulation of Chenopodium quinoa. Plant Physiol Biochem. 2020;151:443–456. doi: 10.1016/j.plaphy.2020.03.050. PubMed DOI

Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development (Cambridge, England) 2000;127(3):595–603. doi: 10.1242/dev.127.3.595. PubMed DOI

Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hattori T. Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J. 2009;58(5):843–856. doi: 10.1111/j.1365-313X.2009.03817.x. PubMed DOI

Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T. Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol. 2010;51(12):2031–2046. doi: 10.1093/pcp/pcq162. PubMed DOI

Yi F, Gu W. High Temporal-resolution transcriptome landscape of early maize seed development. Plant Cell. 2019;31(5):974–992. doi: 10.1105/tpc.18.00961. PubMed DOI PMC

Zhang Z, Tucker E, Hermann M, Laux T. A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell. 2017;40(3):264–277.e264. doi: 10.1016/j.devcel.2017.01.002. PubMed DOI

Zhou X, Liu Z, Shen K, Zhao P, Sun M-X. Cell lineage-specific transcriptome analysis for interpreting cell fate specification of proembryos. Nat Commun. 2020;11(1):1366. doi: 10.1038/s41467-020-15189-w. PubMed DOI PMC

Zogopoulos VL, Saxami G, Malatras A, Angelopoulou A, Jen C-H, Duddy WJ, Daras G, Hatzopoulos P, Westhead DR, Michalopoulos I (2021) Arabidopsis Coexpression Tool: a tool for gene coexpression analysis in Arabidopsis thaliana. iScience 24(8):102848. doi:10.1016/j.isci.2021.102848 PubMed PMC

Comparing the efficiency of six clearing methods in developing seeds of Arabidopsis thaliana