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LEAFY COTYLEDONs (LECs): master regulators in plant embryo development

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Abstract

In plants, somatic embryo development is regulated by a complex group or network of transcription factors (TFs). The LEAFY COTYLEDON (LEC) TFs are significant key regulators that promote the initiation of somatic embryo formation and biological processes of the embryo maturation phase. The LEC gene has been implicated to act as unique regulators in plant embryogenesis, growth and development via diverse signaling pathways. In the present review, we summarize the current advances in our understanding of the LEC TFs in plant biology including embryogenesis. Recent discoveries would be advantageous to unlock the mysteries of LEC TF genes of different molecular mechanisms in plant cells.

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Abbreviations

ABI3 :

ABSCISIC ACID INSENSITIVE3

BBM :

BABY BOOM

FUS3 :

FUSCA3

AGL15 :

Agamous-Like 15

IAA30:

Indole acetic acid inducible 30

LEC :

LEAFY COTYLEDON

PGRs:

Plant growth regulators

PKL :

PICKLE

SD:

Seed development

SE:

Somatic embryogenesis

SERK :

SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASE

TCL:

TRICHOMELESS

TFs:

Transcription factors

WUS :

WUSCHEL

References

  1. Alemanno L, Devic M, Niemenak N, Sanier C, Guilleminot J, Rio M, Verdeil JL, Montoro P (2007) Characterization of leafy cotyledon1-like during embryogenesis in Theobroma cacao L. Planta 227:853–866

  2. Angeles-Núñez JG, Tiessen A (2011) Mutation of the transcription factor LEAFY COTYLEDON 2 alters the chemical composition of Arabidopsis seeds, decreasing oil and protein content, while maintaining high levels of starch and sucrose in mature seeds. J Plant Physiol 168:1891–1900

  3. Arroyo-Herrera A, Gonzalez AK, Moo RC, Quiroz-Figueroa F, Loyola-Vargas V, Rodriguez-Zapata L, Burgeff D’Hondt C, Suárez-Solís VM, Castano E (2008) Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tissue Organ Cult 94:171–180

  4. Baud S, Mendoza MS, To A, Harscoët E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838

  5. Baud S, Kelemen Z, Thevenin J, Boulard C, Blanchet S, To A, Payre M, Berger N, Effroy-Cuzzi D, Franco-Zorrilla JM, Godoy M, Solano R, Thevenon E, Parcy F, Lepiniec L, Dubreucq B (2016) Deciphering the molecular mechanisms underpinning the transcriptional control of gene expression by master transcriptional regulators in Arabidopsis seed. Plant Physiol 171:1099–1112

  6. Bäumlein H, Miséra S, Leurben H, Kölle K, Horstman C, Wobus U, Müller AJ (1994) The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. Plant J 6:379–387

  7. Bouchabké-Coussa O, Obellianne M, Linderme D, Montes E, Maia-Grondard A, Vilaine F, Pannetier C (2013) Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Rep 32:675–686

  8. Boulard C, Fatihi A, Lepiniec L, Dubreucq B (2017) Regulation and evolution of the interaction of the seed B3 transcription factors with NF-Y subunits. Biochim Biophys Acta Gene Regul Mech 1860:1069–1078

  9. Boulard C, Thevenin J, Tranquet O, Laporte V, Lepiniec L, Dubreucq B (2018) LEC1 (NF-YB9) directly interacts with LEC2 to control gene expression in seed. Biochim Biophys Acta 1861:443–450

  10. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002) Ectopic Expression of BABY BOOM Triggers a Conversion from Vegetative to Embryonic Growth. Plant Cell 14:1737–1749

  11. Brand A, Quimbaya M, Tohme J, Chavariagga-Aguirre P (2019) Arabidopsis LEC1 and LEC2 orthologous genes are key regulators of somatic embryogenesis in Cassava. Front Plant Sci 10:673

  12. Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13:624–630

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

  14. Broun P (2004) Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7:202–209

  15. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

  16. Chan A, Carianopol C, Tsai AY, Varatharajah K, Chiu RS, Gazzarrini S (2017) SnRK1 phosphorylation of FUSCA3 positively regulates embryogenesis, seed yield, and plant growth at high temperature in Arabidopsis. J Exp Bot 68:4219–4231

  17. Charlton WA (1996) Lateral root initiation. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 149–174

  18. Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, Herzog M, Vachon G (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol 136:3660–3669

  19. Deng W, Luo KM, Li ZG, Yang YW (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 177:43–48

  20. Devic M, Roscoe T (2016) Seed maturation: simplification of control networks in plants. Plant Sci 252:335–346

  21. Dickinson CD, Evans RP, Nielsen NC (1988) RY repeats are conserved in the 5'-flanking regions of legume seed-protein genes. Nucleic Acids Res 16:371

  22. Domoki M, Györgyey J, Bíró J, Pasternak TP, Zvara Á, Bottka S, Puskás LG, Dudits D, Fehér A (2006) Identification and characterization of genes associated with the induction of embryonic competence in leaf-protoplast-derived alfalfa cells. Biochimet Biophys Acta 1759:543–551

  23. Feeney M, Frigerio L, Cui Y, Menassa R (2013) Following vegetative to embryonic cellular changes in leaves of Arabidopsis overexpressing LEAFY COTYLEDON2. Plant Physiol 162:1881–1896

  24. Fister AS, Landherr L, Perryman M, Zhang Y, Guiltinan MJ, Maximova SN (2018) Glucocorticoid receptor-regulated TcLEC2 expression triggers somatic embryogenesis in Theobroma cacao leaf tissue. PLoS ONE 13:e0207666

  25. Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol 15:121

  26. Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) LEAFY COTYLEDON genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988

  27. Gan LJ, Xia K, Chen JG, Wang SC (2011) Functional characterization of TRICHOMELESS2, a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis. BMC Plant Biol 11:176

  28. Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7:373–385

  29. Goldberg RB, De Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266:605–614

  30. Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Biotechnol 19:138–144

  31. Harada JJ (1997) Seed maturation and control of germination. In: Larkins BA, Vasi IK (eds) Advances in cellular and molecular biology of plants cellular and molecular biology of seed development, vol 4. Kluwer Academic Publishers, Dordrecht, pp 545–592

  32. Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J. Plant Physiol 158:405–409

  33. Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUSLIKE15. Plant Physiol 133:653–663

  34. Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is ex- pressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

  35. Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7:1271–1282

  36. Horstman A, Bemer M, Boutilier K (2017a) A transcriptional view on somatic embryogenesis. Regeneration 4:201–216

  37. Horstman A, Li M, Heidmann I, Weemen M, Chen B, Muino JM, Angenent GC, Boutilier K (2017b) The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-LEC2 network to induce somatic embryogenesis. Plant Physiol 175:848–857

  38. Huang M, Hu Y, Liu X, Li Y, Hou X (2015a) ArabidopsisLEAFY COTYLEDON1 controls cell fate determination during post-embryonic development. Front Plant Sci 6:955

  39. Huang M, Hu Y, Liu X, Li Y, Hou X (2015b) Arabidopsis LEAFY COTYLEDON1 mediates postembryonic development via interacting with PHYTOCHROME-INTERACTING FACTOR4. Plant Cell 27:3099–3111

  40. Ikeda M, Umehara M, Kamada H (2006) Embryogenesis-related genes; its expression and roles during somatic and zygotic embryogenesis in carrot and Arabidopsis. Plant Biotechnol 23:153–161

  41. Irikova T, Grozeva S, Denev I (2012) Identification of BABY BOOM and LEAFY COTYLEDON genes in sweet pepper (Capsicum annuum L.) genome by their partialgene sequences. Plant Grow Regul 67:191–198

  42. Jha P, Kumar V (2018) BABY BOOM (BBM): a candidate transcription factor gene in plant biotechnology. Biotechnol Lett 40:1467–1475

  43. Jia H, Suzuki M, McCarty DR (2014) Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks. Wiley Interdiscip Rev Dev Biol 3:135–145

  44. Jo L, Pelletier JM, Harada JJ (2019) Central role of the LEAFY COTYLEDON1 transcription factor in seed development. J Integ Plant Biol 61:564–580

  45. Jr Rider SD, Henderson JT, Jerome RE, Edenberg HJ, Romero- Severson J, Ogas J (2003) Coordinate repression of regulators of embryogenic identity by PICKLE during germination in Arabidopsis. Plant J 35:33–43

  46. Junker A, Bäumlein H (2012) Multifunctionality of the LEC1 transcription factor during plant development. Plant Signal Behav 7:1718–1720

  47. Junker A, Mönke G, Rutten T, Keilwagen J, Seifert M, Thi TMN, Renou JP, Balzergue S, Viehöver P, Hähnel U, Ludwig-Müller J, Altschmied L, Conrad U, Weisshaar B, Bäumlein H (2012) Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. Plant J 71:427–442

  48. Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005a) Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46:300–311

  49. Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005b) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46:399–406

  50. Keith K, Kraml M, Dengler NG, McCourt P (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6:589–600

  51. Kim HU, Jung SJ, Lee KR, Kim EH, Lee SM, Roh KH, Kim JB (2014) Ectopic overexpression of castor bean LEAFY COTYLEDON2 (LEC2) in Arabidopsis triggers the expression of genes that encode regulators of seed maturation and oil body proteins in vegetative tissues. FEBS Open Bio 4:25–32

  52. Kirkbride RC, Fischer RL, Harada JJ (2013) LEAFY COTYLEDON1, a key regulator of seed development, is expressed in vegetative and sexual propagules of Selaginella moellendorffii. PLoS ONE 8:e67971

  53. Kroj T, Savino G, Valon C, Giraudat J, Parcy F (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130:6065–6073

  54. Kumar V, Van Staden J (2017) New insights into plant somatic embryogenesis: an epigenetic view. Acta Physiol Plant 39:194

  55. Kumar V, Van Staden J (2019) Multi-tasking of SERK-like kinases in plant embryogenesis, growth and development: current advances and biotechnological applications. Acta Physiol Plant 41:31

  56. Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18

  57. Laux T, Jurgens G (1997) Embryogenesis: a new start in life. Plant Cell 9:989–1000

  58. Ledwoń A, Gaj MD (2011) LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Grow Regul 65:157–167

  59. Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci USA 100:2152–2156

  60. Lepiniec L, Devic M, Roscoe TJ, Bouyer D, Zhou DX, Boulard C, Baud S, Dubreucq B (2018) Molecular and epigenetic regulations and functions of the LAFL transcriptional regulators that control seed development. Plant Reprod 31:291–307

  61. Liu Z, Ge XX, Qiu WM, Long JM, Jia HH, Yang W, Dutt M, Wu XM, Guo WW (2018) Overexpression of the CsFUS3 gene encoding a B3 transcription factor promotes somatic embryogenesis in Citrus. Plant Sci 277:121–131

  62. Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Tamagishi K, Fisher RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

  63. Luerssen H, Kirik V, Herrmann P, Miséra S (1998) FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

  64. Manan S, Ahmad MZ, Zhang G, Chen B, Haq BU, Yang J, Zhao J (2017) Soybean LEC2 regulates subsets of genes involved in controlling the biosynthesis and catabolism of seed storage substances and seed development. Front Plant Sci 8:1604

  65. Mangan S, Alon U (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA 100:11980–11985

  66. Marks MD, Feldmann KA (1989) Trichome development in Arabidopsis-thaliana.1. T-DNA tagging of the Glabrous1 gene. Plant Cell 1:1043–1050

  67. Meinke DW (1992) A homoeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258:1647–1650

  68. Meinke DW, Yeung EC (1993) Embryogenesis in angiosperms: development of the suspensor. Plant Cell 5:1371–1381

  69. Meinke DW, Franzmann LH, Yeung EC (1994) Leafy Cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064

  70. Mendes A, Kelly AA, van Erp H, Shaw E, Powers SJ, Kurup S, Eastmond PJ (2013) bZIP67 regulates the omega-3 fatty acid content of Arabidopsis seed oil by activating fatty acid desaturase3. Plant Cell 25:3104–3116

  71. Méndez-Hernández HA, Ledezma-Rodríguez M, Avilez-Montalvo RN, Juárez-Gómez YL, Skeete A, Avilez-Montalvo J, De-la-Peña C, Loyola-Vargas VM (2019) Signaling overview of plant somatic embryogenesis. Front Plant Sci 10:77

  72. Mendoza MS, Dubreucq B, Miquel M, Caboche M, lepineic L, (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett 579:4666–4670

  73. Min L, Hu Q, Li Y, Xu J, Ma Y, Zhu L, Yang X, Zhang X (2015) LEAFY COTYLEDON1-CASEIN KINASE I-TCP15-PHYTOCHROME INTERACTING FACTOR4 network regulates somatic embryogenesis by regulating auxin homeostasis. Plant Physiol 169:2805–2821

  74. Mönke G, Altschmied L, Tewes A, Reidt W, Mock HP, Bäumlein H, Conrad U (2004) Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219:158–166

  75. Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220:412–413

  76. Nic-Can GI, López-Torres A, Barredo-Poll F, Wrobel K, LoyolaVargas VM, Rojas-Herrera R, De-la-Peña C (2013) New Insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS ONE 8:e72160

  77. Nolan KE, Kurdyukov S, Rose RJ (2009) Expression of the SOMATIC EMBRYOGENESIS RECEPTOR-LIKE LINASE1 (SERK1) gene is associated with developmental change in the life cycle of the model legume Medicago truncatulata. J Exp Bot 60:1759–1771

  78. Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94

  79. Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844

  80. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

  81. Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493

  82. Orlowska A, Igielska R, Lagowska K, Kepczynska E (2017) Identification of LEC1, L1Land Polycomb Repressive Complex 2 genes and their expression during the induction phase of Medicago truncatula Gaertn. somatic embryogenesis. Plant Cell Tiss Organ Cult 129:119–132

  83. Parcy F, Valon C, Kohara A, Misera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

  84. Pelletier JM, Kwong RW, Park S, Le BH, Baden R, Cagliari A, Hashimoto M, Munoz MD, Fischer RL, Goldberg RB, Harada JJ (2017) LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc Natl Acad Sci USA 114:6710–6719

  85. Perianez-Rodriguez J, Manzano C, Moreno-Risueno MA (2014) Post-embryonic organogenesis and plant regeneration from tissues: two sides of the same coin? Front Plant Sci 5:219

  86. Peris CIL, Rademacher EH, Weijers D (2010) Green beginnings—pattern formation in the early plant embryo. Plant Dev 91:1–27

  87. Perry SE, Lehti MD, Fernandez DE (1999) The MADS-domain protein AGAMOUS-like 15 accumulates in embryonic tissues with diverse origins. Plant Physiol 120:121–129

  88. Pilarska M, Malec P, Salaj J, Bartnicki F, Konieczny R (2016) High expression of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE coincides with initiation of various developmental pathways in in vitro culture of Trifolium nigrescens. Protoplasma 253:345–355

  89. Pradhan S, Bandhiwal N, Shah N, Kant C, Gaur R, Bhatia S (2014) Global transcriptome analysis of developing chickpea (Cicer arietinumL.) seeds. Front Plant Sci 5:698

  90. Reidt W, Wohlfarth T, Ellerstrom M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21:401–408

  91. Roscoe TJ, Vaissayre V, Paszkiewicz G, Clavijo F, Kelemen Z, Michaud C, Lepiniec L, Dubreucq B, Zhou DX, Devic M (2019) Regulation of FUSCA3 expression during seed development in Arabidopsis. Plant Cell Physiol 60:476–487

  92. Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

  93. Salvo SAGD, Hirsch CN, Buell CR, Kaeppler SM, Kaeppler HF (2014) Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes. PLoS ONE 29:e111407

  94. Santos MO, Romanoa E, Yotoko KSC, Tinoco MLP, Dias BBA, Aragao FJL (2005) Characterization of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Sci 168:723–729

  95. Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620

  96. Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) A leucine rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062

  97. Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987

  98. Shires ME, Florez SL, Lai TS, Curtis WR (2017) Inducible somatic embryogenesis in Theobroma cacao achieved using the DEX-activatable transcription factor-glucocorticoid receptor fusion. Biotechnol Lett 39:1747–1755

  99. Siefers N, Dang KK, Kumimoto RW, Bynum WE, Tayrose G, Holt BF (2009) Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol 149:625–641

  100. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

  101. Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh T, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc Natl Acad Sci USA 105:3151–3156

  102. Suzuki M, Wang HHY, McCarty DR (2007) Repression of the LEAFY COTYLEDON 1/B3 Regulatory Network in Plant Embryo Development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 Genes. Plant Physiol 143:902–911

  103. Tan H, Yang X, Zhang F, Zheng X, Qu C, Mu J, Fu F, Li J, Guan R, Zhang H, Wang G, Zuo J (2011) Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1and LEC1-LIKE in developing seeds. Plant Physiol 156:1577–1588

  104. Tang LP, Zhou C, Wang SS, Yuan J, Zhang XS, Su YH (2016) FUSCA3 interacting with LEAFY COTYLEDON2 controls lateral root formation through regulating YUCCA4 gene expression in Arabidopsis thaliana. New Phyt 213:1740–1754

  105. Tao Z, Shen L, Gu X, Wang Y, Yu H, He Y (2017) Embryonic epigenetic reprogramming by a pioneer transcription factor in plants. Nat 551:124–128

  106. Tao Z, Hu H, Luo X, Jia B, Du J, He Y (2019) Embryonic resetting of the parental vernalized state by two B3 domain transcription factors in Arabidopsis. Nat Plant 5:424–435

  107. Thakare D, Tang W, Hill K, Perry SE (2008) The MADS-domain transcriptional regulator AGAMOUS-Like 15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol 146:1663–1672

  108. To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651

  109. To A, Joubes J, Barthole G, Lecureuil A, Scagnelli A, Jasinski S, Lepiniec L, Baud S (2012) WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell 24:5007–5023

  110. Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492

  111. Tvorogova VE, Fedorova YA, Potsenkovskaya EA, Kudriashov AA, Efremova EP, Kvitkovskaya VA, Wolabu TW, Zhang F, Tadege M, Lutova LA (2019) The WUSCHEL-related homeobox transcription factor MtWOX9-1 stimulates somatic embryogenesis in Medicago truncatula. Plant Cell Tissue Organ Cult 138:517–527

  112. Van Erp H, Kelly AA, Menard G, Eastmond PJ (2014) Multigene engineering of triacylglycerol metabolism boosts seed oil content in Arabidopsis. Plant Physiol 165:30–36

  113. Vicente-Carbajosa J, Carbonaro P (2005) Seed maturation: developing an intrusive phase to accomplish a quiescent state. Int J Plant Sci 49:645–651

  114. Wang SC, Chen JG (2014) Regulation of cell fate determination by single-repeat R3 MYB transcription factors in Arabidopsis. Front Plant Sci 5:133

  115. Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161:1251–1264

  116. Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellins metabolism. Plant Cell 16:1206–1219

  117. Wang H, Guo J, Lambert KN, Lin Y (2007a) Developmental control of Arabidopsis seed oil biosynthesis. Planta 226:773–783

  118. Wang SC, Kwak SH, Zeng QN, Ellis BE, Chen XY, Schiefelbein J, Chen JG (2007b) TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134:3873–3882

  119. Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, Anderson MB, Kaufman LS (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143:1590–1600

  120. West MAL, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5:1361–1369

  121. West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon ldentity in Arabidopsis. Plant Cell 6:1731–1745

  122. Williams EG, Maheswaran G (1986) Somatic embryogenesis: factors influencing coordinated behaviour of cells as an embryogenic group. Ann Bot 57:443–462

  123. Wójcikowska B, Jaskóla K, Gasiorek P, Meus M, Nowak K, Gaj MD (2013) LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta 238:425–440

  124. Xu JJ, Zhang XF, Xue HW (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. J Exp Bot 67:6399–6411

  125. Yang X, Zhang X (2010) Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 29:36–57

  126. Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding Carrot leafy cotyledon 1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42:215–223

  127. Zhang JJ, Xue HW (2013) OsLEC1/OsHAP3E participates in the determination of meristem identity in both vegetative and reproductive developments of rice. J Integr Plant Biol 55:232–249

  128. Zhang SB, Wong L, Meng L, Lemaux PG (2002) Similarity expression patterns of knotted1 and ZmLEC1 during somatic and zygotic embryogenesis in Maize (Zea mays L.). Planta 215:191–194

  129. Zhang S, Liu X, Lin Y, Xie G, Fu F, Liu H, Wang J, Gao S, Lan H, Rong T (2011) Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell Tiss Org Cult 105:29–37

  130. Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–1999

  131. Zheng W, Zhang X, Yang Z, Wu J, Li F, Duan L, Liu C, Lu L, Zhang C, Li F (2014) AtWuschel promotes formation of the embryogenic callus in Gossypium hirsutum. PLoS ONE 9:e87502

  132. Zheng Q, Zheng Y, Ji H, Burnie W, Perry SE (2016) Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiol 172:2374–2387

  133. Zhou LM, Zheng KJ, Wang XY, Tian HN, Wang XL, Wang SC (2014) Control of trichome formation in Arabidopsis by poplar single-repeat R3 MYB transcription factors. Front Plant Sci 5:262

  134. Zhou X, Guo Y, Zhao P, Sun M (2018) Comparative analysis of WUSCHEL-related homeobox genes revealed their parent-of-origin and cell type-specific expression pattern during early embryogenesis in Tobacco. Front Plant Sci 9:311

  135. Zhu S, Wang J, Ye J, Zhu A, Guo W, Deng X (2014) Isolation and characterization of LEAFY COTYLEDON 1-LIKE gene related to embryogenic competence in Citrus sinensis. Plant Cell Tiss Organ Cult 119:1–13

  136. Zhu Y, Xie L, Chen GQ, Lee MY, Loque D, Scheller HV (2018) A transgene design for enhancing oil content in Arabidopsis and Camelina seeds. Biotechnol Biofuels 11:46

  137. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

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Acknowledgements

The authors acknowledge the University of KwaZulu-Natal (UKZN), South Africa for providing financial support. All the authors read and approved the final version of the manuscript. We apologize to all colleagues whose work has not been cited in this manuscript due to space constraints.

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Correspondence to Johannes Van Staden.

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Communicated by Konstantin V. Kiselev.

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Kumar, V., Jha, P. & Van Staden, J. LEAFY COTYLEDONs (LECs): master regulators in plant embryo development. Plant Cell Tiss Organ Cult 140, 475–487 (2020). https://doi.org/10.1007/s11240-019-01752-x

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Keywords

  • Embryogenesis
  • LEAFY COTYLEDON (LEC)
  • Transcription factor
  • Plant biotechnology
  • Seed development