Introduction

Embryogenesis is an essential stage which represents developmental plasticity in higher plant species (Yang and Zhang 2010). Somatic embryogenesis (SE) is an important in vitro regeneration method in modern crop breeding which describes the single cell differentiation into a mature embryo through different development periods (Kumar and Van Staden 2017). In the SE pathway, haploid or diploid somatic cells develop into differentiated plants through different embryological stages (globular, heart, torpedo and cotyledonary-shaped) without fusion of gametes (Williams and Maheswaran 1986; Kumar and Van Staden 2017). In general, two distinct phases are involved in the whole process of plant embryogenesis; early morphogenesis phase which includes the formation of embryogenic cells and tissues, and maturation phase that permit the embryo to enter into a desiccated state (West and Harada 1993; Goldberg et al. 1994; Méndez-Hernández et al. 2019). Studies on the genetic mechanisms confirmed that a number of transcription factors (TFs) have been identified which are responsible for inducing somatic embryogenesis when ectopically expressed. A predominant number of SE-inducing genes encode TFs including SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) (Schmidt et al. 1997; Kumar and Van Staden 2019), BABY BOOM (BBM) (Boutilier et al. 2002; Jha and Kumar 2018), LEAFY COTYLEDON (LEC) (Stone et al. 2001; Gaj et al. 2005), AGAMOUS-LIKE 15 (AGL15) (Harding et al. 2003), WUSCHEL (WUS) (Zuo et al. 2002), and EMBRYO MAKER (Tsuwamoto et al. 2010) have been identified, which are responsible for the induction of differentiated somatic cells and somatic embryo formation. Among the TF genes, the LEC genes are reported to have an important role in controlling several aspects of embryogenesis including embryo development (Gaj et al. 2005; Braybrook and Harada 2008 (Table 1)). The LEC TFs (LEC1, LEC2 and FUSCA3 (FUS3)) are unique regulators of embryogenesis in that they are required to explain the molecular mechanisms for controlling embryo development, morphogenesis and embryo maturation (Harada 2001). The LEC TFs establish environments that encourage the initiation of somatic embryo formation and cellular processes of the maturation phase. The cessation of embryo morphogenesis, synthesis and storage of accumulated macromolecules, acquirement of desiccation tolerance and desiccation of the seed are the major features of the maturation phase (Harada 1997; Vicente-Carbajosa and Carbonaro 2005; Braybrook and Harada 2008). In early embryogenesis, LEC TFs are needed to specify suspensor cell fate and cotyledon identity (Lotan et al. 1998; Meinke et al. 1994; Keith et al. 1994; West et al. 1994; Stone et al. 2001), whereas during late embryogenesis LEC TFs are required for maturation phase for the expression of maturation-specific genes (West et al. 1994; Baumlein et al. 1994). Thus, LEC TFs are candidate gene regulators, which play a key role in controlling many aspects of embryogenesis including morphogenesis and maturation. The LEC1, LEC2 and FUS3 encode two distinct classes of TFs. The LEC1 gene encodes an extensive sequence similarity to the HEMEACTIVATED PROTEIN 3 (HAP3) subunit of the CCAAT-binding TF, an isoform found in seed plants (Lotan et al. 1998; Stone et al. 2001; Kwong et al. 2003; Braybrook and Harada 2008). In Arabidopsis thaliana, based on sequence similarity HAP3 subunits can be divided into two different classes such as LEC1-type and the non-LEC1-type (Lee et al. 2003). Both the LEC1 types are essential for embryogenesis and embryo development (Kwong et al. 2003). The LEC2 and FUS3 genes encodes B3 domain TFs, a DNA-binding motif, which acts in developing seeds (Luerssen et al. 1998; Stone et al. 2001). Ectopic expression of the LEC genes, LEC1 and LEC2 activate SE in vegetative cells and were found to be adequate in embryo development (Lotan et al. 1998; Stone et al. 2001). It was hypothesized that Arabidopsis PICKLE (PKL), which encodes a CHD3-chromatin-remodeling factor, is responsible for repression of the LEC genes during seed germination (Ogas et al. 1999; Rider et al. 2003). Consistent with expression of the LEC genes, PKL mutants accumulate storage products and promote embryonic identity in culture. These embryonic features are repressed by exogenous GA and enhanced by GA synthesis inhibitors (Ogas et al. 1997). The LEC2 and FUS3 TFs activates the genes involved in the accumulation of storage macromolecules in the embryo during maturation. In addition, LEC2 and FUS3 TFs are implicated in repression of GA biosynthesis during seed development (Gazzarrini et al. 2004; Curaba et al. 2004).

Table 1 Showing LECs TF gene and their biological functions in different plant species
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As shown in Fig. 1, LEC1 gene activates YUC10, whereas LEC2 induces YUC2 and YUC4, an auxin biosynthesis enzyme (Stone et al. 2008). The LEC2 gene also induces the IAA30 (negative regulator of auxin signaling) (Braybrook et al. 2006; Kumar and Van Staden 2017; Jha and Kumar 2018). The activation of YUC genes increase the endogenous auxin levels which obviates the necessity for exogenous auxin and provides a critical insight into LEC-mediated SE.

Fig. 1
figure 1

Schematic model which explain the role of LEC TFs in somatic embryogenesis. Ectopic expression of LEC genes induces embryogenesis without exogenous auxin. Based on the articles reviewed we suggest that the endogenous auxin level was increased by LEC1-mediated activation of YUC10 gene and LEC2-mediated activation of YUC2 and YUC4 gene that encodes auxin biosynthesis and IAA30 (negative regular of auxin signaling), which modulate the auxin-mediated signaling during embryogenesis. The FUS3 repressed biosynthesis of GA. Arrows with dotted line indicate transcriptional regulation that molecular mechanisms are not clear and arrows with solid line indicates direct transcriptional regulation by molecular evidence

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The role of LEC genes in embryogenesis have been reported in many plant species such as A. thaliana (Lotan et al. 1998; Stone et al. 2001; Gaj et al. 2005; Wójcikowska et al. 2013), Zea mays (Zhang et al. 2002), Daucus carota hypocotyl (Yazawa et al. 2004), Coffea canephora seedlings (Nic-Can et al. 2013), Medicago sativa protoplasts (Domoki et al. 2006), Medicago truncatula leaves (Orlowska et al. 2017), Theobroma cacao leaf tissue (Alemanno et al. 2007; Fister et al. 2018) and c axillary buds (Brand et al. 2019). Additionally, few studies also revealed diverse biological processes of LECs such as regulation of gene sets, involved in seed development (Pelletier et al. 2017) and for enhancing oil yield in Camelina and Arabidopsis seeds (Zhu et al. 2018). The main purpose of this review is to provide brief insights on the recent discoveries and current advances of the LEC TFs in the area of plant embryogenesis.

Ectopic expression of LEC genes induces embryogenesis without exogenous auxin. Based on the articles reviewed we suggest that the endogenous auxin level was increased by LEC1-mediated activation of YUC10 gene and LEC2-mediated activation of YUC2 and YUC4 gene that encodes auxin biosynthesis and IAA30 (negative regular of auxin signaling), which modulate the auxin-mediated signaling during embryogenesis.

LEC TFs genes are crucial during somatic embryogenesis

SE developmental pathway comprises complex network of cellular processes and expression of several signaling pathways. A considerable number of studies related to molecular genetics confirmed that induction of spontaneous embryogenesis is due to ectopic expression of TF genes (Salvo et al. 2014; Horstman et al. 2017a; Jha and Kumar 2018). LECs TFs are central regulators of plant cell totipotency (Gaj et al. 2005), are responsible for initiation and control of maturation phase during embryogenesis and cause formation of somatic embryos when expressed ectopically (Braybrook and Harada 2008). During embryogenesis the zygote undergoes two different developmental stages i.e. morphogenesis and maturation. In morphogenesis, the basic plant body is established and the embryo is expressed as a shoot (plumule) and root (radicle) axis. (Harada 2001; Laux and Jurgens 1997). During maturation phase several metabolic activities allow the embryo to germinate (Harada 1997). Storage proteins and lipids are stored in protein and lipid bodies throughout the embryo and these are utilized by the growing seedling as a nutrient source.

In addition, at this stage the embryo acquires the ability to withstand desiccation; seeds desiccate at the late development of embryogenesis (Harada 2001).

It is so that the LEC1/2 and FUS3 participate in an important role in controlling several aspects of embryogenesis including early morphogenesis and late maturation phase (Harada 2001; Parcy et al. 1997; Nambara et al. 2000; Kroj et al. 2003; Gaj et al. 2005). The LEC genes are essential to maintain suspensor cell identity during morphogenesis phase in embryogenesis (Meinke and Yeung 1993). A further function during morphogenesis of the LEC genes is the specification of cotyledon identity (Meinke 1992; Meinke et al. 1994; West et al. 1994). Cotyledons are reverting partially to a leaf-like organ and incompletely specified in the absence of LEC gene activity.

During maturation phase, the LEC genes regulate and are responsible for the storage of macromolecule synthesis and accumulation. The LEC genes ectopically expressed in plants accumulates lipids and proteins characteristic of seeds in reproductive and vegetative tissues (Stone et al. 2001, 2008; Mendoza et al. 2005; Baud et al. 2007; Wang et al. 2007a, b). Storage protein synthesis and lipid accumulation is defective in loss-of-function LEC mutants, however, these LEC mutants are involved in the accumulation of starch grains and protein in the distal tips and in basal regions respectively (Meinke et al. 1994; Ikeda et al. 2006). Likewise, a number of researchers have identified that the expression of genes usually active during maturation phase, including genes related to storage lipid and protein accumulation, is defective in LEC mutants (Harada 2001; Bäumlein et al. 1994; Parcy et al. 1997).

The LEC TFs directly target the genes involved in the synthesis of storage macromolecule. The LEC2 and FUS3 TF genes bind with the RY sequence repeats, which is conserved in the 5′ flanking regions of seed protein genes and involved in the regulation of transcription of these genes (Dickinson et al. 1988; Kroj et al. 2003; Reidt et al. 2000; Monke et al. 2004; Braybrook et al. 2006). During maturation phase, ABSCISIC ACID INSENSITIVE3 (ABI3) interacts with LEC genes to regulate the seed protein genes (Kroj et al. 2003; To et al. 2006). Activation of LEC1 seed protein gene is dependent on the ABI3 and other LEC genes. Ectopic expression of LEC1 activates the ABI, LEC2 and FUS3 genes (Kagaya et al. 2005a).

A complex relationship among the LEC TFs for the regulation of embryo maturation has been shown in Fig. 2. During embryo maturation phase LEC TFs exhibit complex regulatory interrelationships to activate several genes to induce maturation. The LEC2 activates both LEC1 and FUS3 (Stone et al. 2008), whereas, LEC1 activates LEC2 and FUS3 (Kagaya et al. 2005b; To et al. 2006). LEC TFs interact with GA; LEC2 directly induces and activates AGL15 (Braybrook et al. 2006). The AGL15 positively activates GA degrading enzyme GA3ox2 (Wang et al. 2004; Kumar and Van Staden 2017). The FUS3 represses the GA3ox1 and GA3ox2 (GA biosynthesis genes) (Gazzarrini et al. 2004; Curaba et al. 2004). PKL represses LEC genes in seedlings (Ogas et al. 1997; Rider Jr. et al. 2003). PKL mutants express LEC genes ectopically and the overexpression of LEC genes is enhanced by GA synthesis inhibitors. However, PKL-mediated repression of the maturation process is still unclear. These characteristics revealed that the LEC TF genes play an essential role in controlling embryogenesis processes in plants. The LEC genes have distinct differences, although they share similar mutant phenotypes. Finally, the LEC genes are candidate markers that coordinate embryogenesis being involved in both morphogenesis and maturation stages.

Fig. 2
figure 2

Schematic overview of regulation of the embryo maturation phase by LEC TFs. During embryo maturation phase LEC TFs exhibit complex regulatory interrelationship to activate several genes to induce maturation. The LEC2 activates both LEC1 and FUS3 (Stone et al. 2008), whereas, LEC1 activates LEC2 and FUS3 (Kagaya et al. 2005b; To et al. 2006). LEC TFs interact with GA; LEC2 directly induces and activates AGL15 (Braybrook et al. 2006). The AGL15 positively activates GA degrading enzyme GA3ox2 (Wang et al. 2004; Kumar and Van Staden 2017). The FUS3 represses the GA3ox1 and GA3ox2 (GA biosynthesis genes) (Gazzarrini et al. 2004; Curaba et al. 2004). PKL represses LEC genes in seedlings (Ogas et al. 1997; Rider et al. 2003). pkl mutants express LEC genes ectopically and the overexpression of LEC genes is enhanced by GA synthesis inhibitors. However, PKL-mediated repression of maturation process is still unclear

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Other transcription factor genes controlling plant embryogenesis

SE consists of various developmental phases which initiates with embryonic induction. While the cells are in induction phase, several genes are functional, possibly due to biotic or abiotic stresses or extrinsic hormones. The induction phase can further be classified into three sub stages: embryogenic dedifferentiation, totipotency expression and embryogenic commitment. Cell dedifferentiation is a cellular regression process in which mature cells are converted into transient stages.

As discussed above, LEC genes have been found to be key regulators for embryogenesis when ectopically expressed. However, other TF genes have also been recognized to promote embryogenesis which includes SERK (Schmidt et al. 1997; Hecht et al. 2001), BBM (Boutilier et al. 2002), AGL15 (Harding et al. 2002), WUS (Zuo et al. 2002), and EMBRYO MAKER (Tsuwamoto et al. 2010).

SERK role is identified during embryogenesis in several plant species such as A. thaliana (Hecht et al. 2001), Z. mays (Zhang et al. 2011), M. truncatula (Nolan et al. 2009), T. cacao (Santos et al. 2005) and T. nigrescens (Pilarska et al. 2016). In a study on Arabidopsis, by Hecht et al. (2001), AtSERK1 was found to be highly expressed during early embryogenesis. The study suggested that AtSERK1 gene is initially expressed during megasporogenesis in the megaspore and in cells of embryo sac till fertilization stage. However, least expression of the same gene has been found in matured vascular tissues. ZmSERK1 and ZmSERK2 genes isolated from Z. mays, has been found to express during embryogenesis (Zhang et al. 2011). Interestingly, ZmSERKs genes expression are associated to embryo development and hormone signaling. These studies indicates that SERK gene is involved in cell to embryonic transition in plant cells.

WUS encodes the homoeodomain TF, reported to play an important role in plant embryogenesis. It has been observed that WUS is positively up-regulated during SE in various plant species (Zuo et al. 2002; Zheng et al. 2014; Tvorogova et al. 2019). Ectopic expression of WUS gene was shown to be involved in vegetative-to-embryonic transition in all tissues (leaf petiole, leaves, stem and root), without adding exogenous growth hormones in A. thaliana (Zuo et al. 2002). In C. canephora, overexpression of WUS significantly enhanced the embryo development up to 400%, and also increased the SE in a heterologous system, however exogenous PGRs were essential for the initiation of SE (Arroyo-Herrera et al. 2008).

A. thaliana WUS (AtWUS) significantly increased embryogenic callus formation (47.75%) in G. hirsutum (cotton), when ectopically expressed (Zheng et al. 2014), and also positively upregulated LEC1, LEC2 and FUS3 in the embryogenic callus. Similarly, Bouchabké-Coussa et al. (2013) also revealed that WUS overexpression significantly promoted (×3) embryogenic capacity and triggered in vitro regeneration competence in cotton when WUS was expressed ectopically. However, these researchers also examined that WUS overexpression resulted in the initiation of embryo-like structures (abnormal) and that leaf-like structures developed on the somatic embryos (Bouchabké-Coussa et al. 2013).

In tobacco, Zhou et al. (2018) uncovered a novel function of WOXs in regulating embryo patterning, and confirmed by expression pattern analysis that WOX2 and WOX9 are essential for early embryo patterning. In a recent report with M. truncatula, it was showed that the WOX9 homolog, MtWOX9-1, participates in embryogenesis and its overexpression enhances embryogenic capacity by changing the expression levels of various SE-associated genes (Tvorogova et al. 2019). These findings confirmed that WUS and WOX family members have an important impact on improving SE competence in plant cells.

BBM TF is a master regulator, which induces embryo development without any exogenous PGRs (Boutilier et al. 2002; Jha and Kumar 2018). In a breakthrough report, it was observed that BBM transcriptionally regulates LEC1/2, ABI3 and FUS3 network during plant embryogenesis (Horstman et al. 2017b). This observation indicates that LEC1 and FUS3 are crucial for embryo development, where as ABI3 and LEC2 positively regulates BBM-mediated SE. However, it is a context and dose-dependent mechanism. In a breakthrough report by Boutilier et al. (2002), it was found that in Arabidopsis an ortholog gene (AtBBM) and in B. napus two ortholog genes (BnBBM1 and BnBBM2) were recognized and it was revealed that overexpression of these ortholog genes encourage embryo development. A transgene constructs 35S::BBM and UBI::BBM were used for transformation in Arabidopsis and B. napus respectively and responsible for cotyledon-shaped embryo development on post-germination organs. Interestingly, in P. tomentosa, overexpression of BBM-mediated embryogenesis significantly improved regeneration pathway (Deng et al. 2009). BBM induces embryo development from P. tomentosa calli, when expressed ectopically. Approximately 12 embryo were developed from 6 calli after 28 days, however, among 12 only 6 embryo survived and developed into complete plantlets (Deng et al. 2009). Similarly, in T. cacao, an ortholog gene (TcBBM) has been identified, which is found to promote the vegetative to embryonic transition of T. cacao somatic cells (Florez et al. 2015).

Expression level of TcBBM gene was found throughout the embryogenesis process including several stages such as globular-stage, heart-stage, early and late torpedo stage and cotyledonary stages. These expression levels led to phenotype in T. cacao, without any exogenous PGRs for direct embryogenesis, however, TcBBM overexpression enhanced embryonic potential significantly. Overall, these findings showed that TcBBM transcriptional level plays a vital role in embryogenesis and it could use as marker gene in T. cacao tissue for embryonic growth (Florez et al. 2015).

AGL15 encodes a MADS domain TF that is expressed during embryogenesis, although not exclusively (Heck et al. 1995; Rounsley et al. 1995; Perry et al. 1999; Wang et al. 2004; Zheng et al. 2016). In Arabidopsis, AGL15 can stimulate SE and lead to extended periods (over 12–19 years to date), when expressed ectopically (Harding et al. 2003; Thakare et al.2008; Zheng et al. 2016). A transgene (35S promoter:AGL15), promotes SE from apical region of shoots which is germinated in the medium supplemented with 2,4-D (Harding et al. 2003; Thakare et al.2008). In addition, overexpression of AGL15-like TF gene is responsible for early embryogenesis in Zea mays (Salvo et al. 2014). Moreover, gene encoding putative ortholog, GmAGL15 (isolated from Glycine max) can enhance embryo development in Arabidopsis (Thakare et al. 2008). However, loss-of-function alleles of agl15 showed significant reduction in SE (Thakare et al. 2008). Finally, the different TF genes are master regulators that coordinate SE being involved in both early and late embryo development.

LEC TFs gene mediated oil content accumulation

Oilseed crop improvement is one of the major objectives to fulfil the ever-increasing oil needs by humans and for biodiesel production. A number of plants accumulate oils in the seeds with several beneficial effects. Mainly plant oil is synthesized as triacylglycerols (TAGs) from fatty acyl-CoA and glycerol-3-phosphate (Ohlrogge and Browse 1995; Shen et al. 2010).

Seed oil content in plants is controlled by several phases in the oil biosynthetic pathway. Oilseed accumulation and biosynthesis are influenced by various genes which are involved directly or indirectly in embryo or seed development (Wang et al. 2007a, b; Shen et al. 2010; Tan et al. 2011; Zhu et al. 2018). In A. thaliana, two important TFs LEC1 and WRINKLED1 (WRI1) have been found which are involved in the regulation of oil accumulation (Lotan et al. 1998; Cernac and Benning 2004). Several studies by pioneer scientists have been documented that overexpression of TFs enhance the oil production in plants when compared to the overexpression of pathway enzymes (Broun 2004; Grotewold 2008; Van Erp et al. 2014). The LEC TFs are key regulators of embryogenesis and are also involved in fatty acid biosynthesis by increasing the expression of genes.

In Zea mays (maize), ZmLEC1 (maize LEC1) is overexpressed as a key regulator and increases the seed oil production (Shen et al. 2010). The ZmLEC1 gene homolog exhibited 41% identity to Arabidopsis LEC1 in amino acid sequence. Overexpression of ZmLEC1 enhanced the oil content by 48.7% in transgenic maize, however, seed germination and leaf growth reduced significantly (Shen et al. 2010). The transgenic leaves were 40–50% shorter, and were narrow and dark green in colour. Transgenic ZmLEC1 seedlings shoot and root growth were slower, resulting in reduced height of the plant in the field.

In a recent promising report, LEC gene was shown to increase oil production in Arabidopsis and Camelina seeds (Zhu et al. 2018). By using Agrobacterium-mediated floral dip method ZmLEC1 binary vector were constructed, driven by seed-specific serine carboxypeptidase-like (SCPL17) and acyl carrier protein (ACP5) promoters and introduced into Arabidopsis and Camelina for expression. The overexpression of ZmLEC1 enhanced the total oil content by < 20% in Arabidopsis and < 26% in Camelina mature seeds (Zhu et al. 2018). Interestingly, there was no phenotypic variation or abnormal growth identified throughout the life cycle of both the plants. These results suggest that ZmLEC1, a master regulator, trigger and increases the oil content in Arabidopsis and Camelina seeds and might be useful for the enhancement of oil production in different crops or oilseed crop improvement. Similarly, in Brassica napus, overexpression of BnLEC1 and Bn LEC1-like TFs significantly increases the total seed oil content by 2–20% in transgenic seeds without any abnormal effects on agronomic traits (Tan et al. 2011). In a report by Angeles-Núñez and Tiessen (2011), they proposed that overexpression of LEC2 TF reduced the seed oil content by 30% while maintaining high levels of sucrose (140%) and starch (> fivefold more) in transgenic Arabidopsis seeds. Future research with more extensive analysis may help to understand the molecular mechanisms on how LEC genes are involved in the expression of genes for fatty acid biosynthesis.

LEC crucial for seed development

Seed development (SD) is a critical and complex phase of the higher plant life cycle. A seed comprises three different regions (filial embryo, filial endosperm and maternal seed coat) with distinct variation on a common genotype (Jo et al. 2019). Furthermore, each region contains distinct subregions, cell and tissues. SD process starts with a double fertilization event that generate the zygote and endosperm (Goldberg et al. 1994; Harada 2001). Many TFs have been shown to express and regulate diverse processes during SD (Pradhan et al. 2014; Jia et al. 2014; Devic and Roscoe 2016; Jo et al. 2019). Among the TFs involved in SD, LEC1 has been considered to be a central regulator of SD (Harada 2001; To et al. 2006; Braybrook and Harada 2008; Pelletier et al. 2017; Jo et al. 2019). LEC1 TF acts sequentially and controls diverse processes at several stages of SD (Pelletier et al. 2017). During SD, LEC1 acts indirectly to regulate diverse processes by activating TFs controlling structural genes, however, LEC1 also regulate directly by establishing a feed-forward loop (FFL) network with association of other TFs (Mangan and Alon 2003). In addition, LEC1 also interacts with several other TFs and activates a particular set of genes during SD (Huang et al. 2015b).

LEC1 is also positively involved in chloroplast biogenesis and photosynthesis during SD (Pelletier et al. 2017; Jo et al. 2019). In Arabidposis and Glycine max (soybean) embryos, LEC1 TF transcriptionally activates and expressed a genes encoding the light-reaction components of photosystems I and II and other set of genes involved in photosynthesis and chloroplast biogenesis (Pelletier et al. 2017). It was also identified that LEC1 TF also regulates and control endosperm development (Lotan et al. 1998). In rice, LEC1 control endosperm development through its interaction with AP2 TFs (Zhang and Xue 2013; Xu et al. 2016).

It was found that LEC1 may regulate directly or indirectly different TFs to regulate gene sets involved in early and late stages of SD (Junker et al. 2012; Pelletier et al. 2017; Jo et al. 2019). The LEC1 directly regulates the LEC2, ABI3 and FUS3 TFs, which all are master regulators of seed maturation (Santos-Mendoza et al. 2008; Braybrook and Harada 2008; Boulard et al. 2017, 2018). It confirms that LEC1 transcriptionally regulates ABI3 and FUS3 and together they form a feed-forward loop (FFL) network, a three-gene pattern and regulates a target gene (Mangan and Alon 2003). Similarly, LEC1 directly regulates WRINKLED1 (WRI1) (TF which plays a key role in seed maturation), and make a FFL network and directly regulate genes involved in the fatty acid accumulation during SD in Arabidopsis (Baud et al. 2007; To et al. 2012; Jo et al. 2019). Moreover, LEC1 TF also control SD indirectly by regulating the expression of TFs that independently control SD.

Few studies suggested that LEC1 may interact with other TFs to regulate diverse development processes during SD (Parcy et al. 1997; To et al. 2006; Pelletier et al. 2017; Jo et al. 2019). In a recent report published in PNAS, they propose that LEC1 acts sequentially and interacts with different TFs and respond to different developmental signals during seed development (Pelletier et al. 2017). LEC1 interacts with LEC2, ABI3 and FUS3 TFs and control gene expression in seeds and are involved in the regulation of diverse processes during seed maturation (Devic and Roscoe 2016; Boulard et al. 2018; Lepiniec et al. 2018).

LEC1 control the maturation phase by interacting with B3 and bZIP (basic leucine zipper TF) TFs which accumulate during SD (Mendes et al. 2013; Baud et al. 2016).

In addition, LEC1 interacts with PHYTOCHROME INTERACTING FACTOR4 (PIF4) (a transcriptional modulator), which is responsible for the expression of hypocotyl elongation related genes through G box element (Huang et al. 2015b). LEC1 also interacts with TCL2 to repress trichome formation during embryogenesis (Huang et al. 2015a). Finally, the interaction of LEC1 with many other TFs provides an outline to define how LEC1 regulate and express distinct gene sets during different phases of SD. In future, LEC1 interaction with all TFs and their impact on LEC1 could provide novel insights into the multitasking of LEC1 during SD. In A. thaliana, FUS3 phosphorylation at SnRK1 (conserved eukaryotic kinase complex) sites positively regulates seed yield and plant growth at heat stress (Chan et al. 2017). They concluded that FUS3 phosphorylation plays an important role for SD and plant growth at high temperature. However, the molecular mechanism by which FUS3 regulates is still elusive. Finally, LEC1 TF has been identified as a central regulator of SD, however, very little is known about the mechanisms by which LEC1 controls and regulates diverse biological processes of SD.

Multi-functionality of LEC TFs during plant development

The LEC TFs acts as a master regulator and are involved in diverse functions including plant embryogenesis, growth and development. In A. thaliana, Junker and Baumlein 2012 and Junker et al. 2012 identified that LEC1 TF affects light and brassinosteroid (BR) signaling during embryogenesis. In addition, LEC1 expression has also been detected in etiolated seedlings (Warpeha et al. 2007; Siefers et al. 2009; Junker et al. 2012).

Lateral root development is critical for higher plants and is responsible for the uptake of water and nutrient acquisition for the growth and development of plants (Charlton 1996; Tang et al. 2016). Embryonic master regulators LEC2 and FUS3 are involved in the lateral root formation by regulating YUC functions (Tang et al. 2016). In A. thaliana, a FUS3 and LEC2 complex function synergistically and activates auxin biosynthesis and YUC gene during lateral root formation. However, expression of FUS3 during lateral root formation is activated by LEC2 (Tang et al. 2016). In future, more extensive studies will hopefully provide novel findings for the better understanding of the molecular mechanisms of lateral root formation.

A number of studies have been reported that during post-embryonic development cell fate determination is controlled by TFs (Peris et al. 2010; Perianez-Rodriguez et al. 2014). Few researchers documented a significant role of LEC1 in post-embryonic cell differentiation, including formation of trichomes, mesophyll cells and vascular tissue (Junker and Baumlein 2012; Junker et al. 2012). The regulation of trichome formation by different TFs has been well studied by several researchers (Marks and Feldmann 1989; Oppenheimer et al. 1991; Wang and Chen 2014; Zhao et al. 2008; Zhou et al. 2014). Huang et al. (2015a) documented that LEC1 is positively involved in cell fate determination during post-embryonic development in A. thaliana. They found that LEC1 interacts in vitro with transcription repressors such as TRICHOMELESS1/2 (TCL1/2), CAPPICE (CPC) and ENHANCER OF TRY AND CPC1 (ETC1) to repress trichome formation. It was identified that TCL1 was highly expressed in developing seeds, whereas TCL2 in cotyledons (Wang et al. 2007a, b; Gan et al. 2011). The interaction with these repressors provides a mechanism by which LEC1 regulates cell fate determination.

In a recent breakthrough report by Tao et al. (2019), they discovered that LEC2 and FUS3 TFs are involved in expression of key flowering gene and embryonic resetting in Arabidopsis. The LEC2 and FUS3 TFs compete against VAL1 and VAL2 (epigenome readers) to disrupt the Polycomb silencing during early embryogenesis. Furthermore, LEC2 and FUS3 recruit the FRIGIDA (scaffold protein) in order to establish an active chromatin state, resulting in the activation of FLC (FLOWERING LOCUC C, a floral repressor) and erasing the parental memory in early somatic embryos during winter cold. However, LEC2 and FUS3 were silenced during post-embryonic phase (Tao et al. 2019). Reprogramming of epigenetic mechanisms during embryogenesis by LEC TF is well reported (Tao et al. 2017).

Further research will help to unlock the different biological and molecular mechanism underlying these processes. These results suggest that over-expression of LEC gene has been used for multifunction in different plant species. Increasing current advances and better understanding of the mechanism of LEC genes will lead to new opportunities and development of different biological applications.

Conclusions and future perspectives

The findings presented reveal that the LEC transcription factor genes have emerged as a master regulator that controls diverse aspects of somatic embryogenesis and has potential application in the plant biology. The LEC TFs are used as candidate markers to define the molecular mechanisms that control the initiation and maturation phase of SE. The expression of the LEC gene provides clear evidence of its role in embryogenesis and diverse developmental signaling pathways including oil content accumulation, cell fate determination, lateral root development and chloroplast biogenesis and photosynthesis during seed development. The LEC gene acts as a master regulator to participate in initiation and maturation of somatic embryos but how the LEC-mediated cellular process initiates the maturation phase is still unclear. In addition, how the LEC TFs control signaling transmission specificity to regulate initiation and maturation of somatic embryo at the molecular level remains unclear. In addition, LEC also acts as a pioneer TF gene, which activates different sets of genes and controls diverse biological processes during SD. However, we are only at the beginning to understand the potential insight and molecular mechanism by which LEC1 regulates diverse functions of SD. Recent discoveries have explored the multiple roles of LEC TFs in diverse aspects of plant growth and development. However, a few future challenges still need to be clarified such as LEC1 and LEC2 are involved in the diverse signaling pathways related to embryogenesis including embryo morphogenesis and maturation, but how these pathways are regulated remains unclear. In addition, how is the specificity of these LEC TFs obtained? Apart from known processes, what additional physiological and biological processes are regulated by LEC TFs? The underlying molecular mechanism by which LEC regulates diverse biological processes of SD is still unclear. Therefore, research should shed some light on how these LEC TFs control embryogenesis and several aspects of plant dynamics. In order to decode these regulatory networks, a single-molecule imaging technology will be required to understand the diverse functions of individual LECs in different signaling pathways. Together, structural studies of different LECs may open new roadmaps for better understanding their signaling specificity and developmental plasticity. It would also help to find new insights into the molecular mechanisms and unexplored signaling pathways for the better understanding of the functions of LEC TFs in plant cells.