ABSTRACT

Plants react to wounding through the activation of both defense and repair pathways, but how these two responses are coordinated is unclear. Here, we put forward the hypothesis that diverse members of the subfamily X of the plant-specific ethylene response factor (ERF) transcription factors coordinate stress signaling with the activation of wound repair mechanisms. Moreover, we highlight the observation that tissue repair is strongly boosted through the formation of a heterodimeric protein complex that comprises ERF and transcription factors of the GRAS domain type. This interaction turns ERFs into highly potent and stress-responsive activators of cell proliferation. The potency to induce stem cell identity suggests that these heterodimeric transcription factor complexes could become valuable tools to increase crop regeneration and transformation efficiency.

Introduction

Plants have evolved many different strategies to cope with distinct types of biotic and abiotic stresses, as well as with injury through wounding. These strategies have likely been developed because of their immobile lifestyle. Wounding threatens plant survival, especially if it occurs in the stem that holds the vascular tissue that is used for the transport of nutrients and water, as the stem connects the shoot and leaves with the flowers and fruits (Melnyk, 2017). Additionally, wounds represent possible entry sites for pathogens. At the cellular level, plants respond to wounding by activation of their defense systems (Savatin et al., 2014). Physiological responses include the repair and reinforcement of the cell wall and the activation of wound-signaling pathways. This occurs through induction of both local and systemic defense-related proteins and activation of hormones related to wounding, such as ethylene and jasmonic acid (JA) (León et al., 2001; Sasaki et al., 2002). In parallel, the plant initiates mechanisms of wound healing, which often imply a local reactivation of cell division (Heyman et al., 2016; Sena et al., 2009).

Whereas the signaling cascades used by plants to prevent infection following wounding have been well documented, how these pathways communicate with cell repair mechanisms is unclear. Based on recent findings, we speculate below that the unique subgroup X of transcription factors of the ethylene response factor (ERF) family coordinates stress signaling with wound healing. Moreover, we highlight that – at least for the process of wound healing – the activity of these transcription factors is fine-tuned and controlled through their heterodimerization with transcription factors of a distinct protein family. This heterodimerization turns the ERFs into highly potent cell division activators. Finally, we discuss the use of these heterodimeric transcription factors to improve plant regeneration.

The ERF family of transcription factors

The Arabidopsis thaliana genome encodes more than 65 gene transcription factor families, with some comprising over 100 family members (Mitsuda and Ohme-Takagi, 2009; Riaño-Pachón et al., 2007). Among these different families, the ERF family of plant-specific transcription factors constitutes one of the largest (Nakano et al., 2006). The discovery of the ERF family is connected to the characterization of the homeotic APETALA2 (AP2) gene, a putative nuclear protein that harbors an essential 68-amino-acid repeat motif that was designated the AP2 domain and contains DNA-binding activity (Jofuku et al., 1994; Ohme-Takagi and Shinshi, 1995). The gene was identified through its ability to promote the establishment of the floral meristem: mutations in this locus result in the transformation of sepals into leaves, and petals into stamenoid organs that produce pollen, or even cause sepals to be transformed into carpels which bear the ovules (Bowman et al., 1989; Bowman et al., 1991; Kunst et al., 1989). Since then, the number of identified AP2-type genes increased noticeably across the plant kingdom, counting 147 in Arabidopsis thaliana and up to 210 in Zea mays (Guo et al., 2016; Lata et al., 2014; Liu et al., 2013; Nakano et al., 2006; Rao et al., 2015).

The Arabidopsis thaliana ERF family can be subdivided into four main groups: AP2 (18 members), RAV (six members), ethylene-responsive element binding (EREB)-dehydration-responsive element-binding (DREB) proteins (122 members), and a group with the single member APETALA 2 FAMILY PROTEIN INVOLVED IN SALICYLIC ACID MEDIATED DISEASE DEFENSE 1 (Nakano et al., 2006). The 18 members of the AP2 subgroup are hallmarked by the presence of two AP2 domains (Fig. 1A). Besides AP2 itself, PLETHORA (PLT) proteins comprise a well-studied subfamily of the AP2-type transcription factors. The PLT transcription factors were originally identified as essential regulators that control stem cell activity in the Arabidopsis thaliana root (Aida et al., 2004; Santuari et al., 2016). Additionally, PLTs orchestrate phyllo- and rhizo-taxis during plant development (Hofhuis et al., 2013; Prasad et al., 2011); together with AINTEGUMENTA (ANT), another AP2-type transcription factor, they control shoot apical meristem function (Mudunkothge and Krizek, 2012; Nole-Wilson et al., 2005). Thus, the AP2 subfamily contains several key regulators that control different developmental processes during plant growth.

Fig. 1.

Schematic overview of the structural organization of the different ERF subfamilies. (A) Plants have three major groups of ERF transcriptions factors: AP2, EREB/DREB, and RAV. The number of respective family members in Arabidopsis thaliana is listed in brackets. Conserved amino acid motifs (AP2 and B3) that mark the different groups are indicated. Developmental and stress processes controlled by the different ERF classes are listed on the right. (B) Schematic representation of the ERF subfamily X protein members, including the subfamily-specific conserved motif and possible posttranslational modification sites. AA, Amino Acid; P, phosphorylation site as described for ERF110 (Li et al., 2012); Ub, ubiquitylation site as reported for ERF115 (Walton et al., 2016).

Fig. 1.

Schematic overview of the structural organization of the different ERF subfamilies. (A) Plants have three major groups of ERF transcriptions factors: AP2, EREB/DREB, and RAV. The number of respective family members in Arabidopsis thaliana is listed in brackets. Conserved amino acid motifs (AP2 and B3) that mark the different groups are indicated. Developmental and stress processes controlled by the different ERF classes are listed on the right. (B) Schematic representation of the ERF subfamily X protein members, including the subfamily-specific conserved motif and possible posttranslational modification sites. AA, Amino Acid; P, phosphorylation site as described for ERF110 (Li et al., 2012); Ub, ubiquitylation site as reported for ERF115 (Walton et al., 2016).

RAV-type transcription factors respond transcriptionally to touch-related stimuli (Kagaya and Hattori, 2009). In contrast to the AP2-type transcription factors, RAVs possess a single AP2 domain and a second conserved DNA-binding domain, which is located at their C-terminus and designated B3 (Fig. 1A) (Kagaya et al., 1999). A single AP2 domain can also be found in the members of the EREB proteins (Fig. 1A), which were identified as factors that mediate the ethylene response through recognition of the consensus GCC-motif within target gene promoters (Fujimoto et al., 2000; Ohme-Takagi and Shinshi, 1995). The DREB subfamily within the EREB class is defined by their ability to activate target gene expression upon dehydration (Ingram and Bartels, 1996; Kizis et al., 2001). As suggested by their name, DREB transcription factors control the expression of genes that hold a drought-responsive cis-acting element, although also they regulate low temperature- and cold-responsive genes (Baker et al., 1994; Jiang et al., 1996; Liu et al., 1998).

The EREB-DREB subfamily X

Phylogenetic clustering of the 122 Arabidopsis EREB-DREB members led to their classification into 12 subgroups, namely I to X, VI-L and Xb-L (Nakano et al., 2006). Here, we review the features of the members of the X subfamily (ERF108 to ERF115), whose hallmark is a conserved N-terminal sequence (Figs 1B and 2) and discuss their participation in wound signaling and tissue repair.

Fig. 2.

Phylogenetic tree of the Arabidopsis thaliana ERF subfamily X. The phylogenetic tree was constructed using the Maximum Likelihood Method (cpREV+G, 500 bootstrap iterations; only bootstrap values>50 are shown) with Mega software (v5.1), based on a multiple sequence alignment (generated with Clustal Omega) of the AP2 domains of ERF family X protein members. For each family member, the Arabidopsis Genome Initiative (AGI) locus code, the alternative gene name (alias), and the subfamily conserved amino acid motif is given. N.A., not applicable.

Fig. 2.

Phylogenetic tree of the Arabidopsis thaliana ERF subfamily X. The phylogenetic tree was constructed using the Maximum Likelihood Method (cpREV+G, 500 bootstrap iterations; only bootstrap values>50 are shown) with Mega software (v5.1), based on a multiple sequence alignment (generated with Clustal Omega) of the AP2 domains of ERF family X protein members. For each family member, the Arabidopsis Genome Initiative (AGI) locus code, the alternative gene name (alias), and the subfamily conserved amino acid motif is given. N.A., not applicable.

ERF108

ERF108, also known as RELATED TO APETALA2.6 (RAP2.6), was identified as a transcription factor that can be induced by JA (Wang et al., 2008), which is in line with studies that demonstrate that its transcription is induced by pathogens (Fig. 3) (He et al., 2004). In order to find novel components that are involved in wound signal perception and JA signaling, a screen for mutants that display constitutive ERF108 expression was performed and resulted in the identification of a mutation in the MECHANOSENSITIVE CHANNEL OF SMALL CONDUCTANCE-LIKE 10 (MSL10) gene (Zou et al., 2016). This mutant displays characteristic features of the JA response, such as accumulation of anthocyanin pigments and shorter petioles. These results corroborated the observation that ERF108 is a target of the JA signaling pathway. Apart from JA, other stress signals, such as abscisic acid (ABA), heat, drought, sorbitol and salt, significantly induce ERF108 expression (Krishnaswamy et al., 2011; Zhu et al., 2010). Upon overexpression of ERF108, plants develop more secondary branches and are dwarfed. Moreover, these transgenic plants display hypersensitivity to ABA and osmotic stress during seed germination and early seedling growth stages. Thus, it appears that ERF108 represents a stress-inducible transcript required for stress adaptation. Interestingly, ERF108 is phylogenetically related to the tobacco WOUND-RESPONSIVE AP2-LIKE FACTOR 1 (WRAF1) and WRAF2 proteins. Both bind the vascular system-specific and wound-responsive cis-acting element (VWRE) that has been mapped within the promoter of the wound-induced tpoxN1 peroxidase gene (Sasaki et al., 2006; Sasaki et al., 2007). This indirectly suggests that ERF108 might also participate in wound healing (Fig. 3).

Fig. 3.

Overview of the ERF X subfamily members and their function in wound response and tissue repair. Lines connect the different ERF members with upstream activating cues and downstream events. The distinct ERF subfamily members respond to a diverse set of wound-induced stimuli: pathogen attacks, abiotic stress signals (such as cold), jasmonic acid (JA), reactive oxygen species (ROS), abscisic acid (ABA), ethylene, salicylic acid (SA) and tissue damage. Downstream events include the activation of a ROS burst, resistance to waterlogging and drought, bolting time control, activation of vascular thickening, shoot branching, lateral root primordia (LRP) initiation, tissue regeneration following wounding, spontaneous callus formation and root stem cell proliferation. Note that for ERF112 no upstream activating cue or downstream function is appointed, as no such data are available to date. The color scale at the bottom indicates the putative gradation of involvement of the ERF family members in stress (blue) and wounding (orange) response.

Fig. 3.

Overview of the ERF X subfamily members and their function in wound response and tissue repair. Lines connect the different ERF members with upstream activating cues and downstream events. The distinct ERF subfamily members respond to a diverse set of wound-induced stimuli: pathogen attacks, abiotic stress signals (such as cold), jasmonic acid (JA), reactive oxygen species (ROS), abscisic acid (ABA), ethylene, salicylic acid (SA) and tissue damage. Downstream events include the activation of a ROS burst, resistance to waterlogging and drought, bolting time control, activation of vascular thickening, shoot branching, lateral root primordia (LRP) initiation, tissue regeneration following wounding, spontaneous callus formation and root stem cell proliferation. Note that for ERF112 no upstream activating cue or downstream function is appointed, as no such data are available to date. The color scale at the bottom indicates the putative gradation of involvement of the ERF family members in stress (blue) and wounding (orange) response.

ERF109

ERF109 is also known as REDOX RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) (Khandelwal et al., 2008). Similar to ERF108, ERF109 expression is induced by many different abiotic stresses: salt, drought, cold, ultraviolet B, heat, osmotic stress, as well as hormones such as ABA and JA (Fig. 3) (Gadjev et al., 2006; Matsui et al., 2008; Toufighi et al., 2005; Wang et al., 2008). Its transcription is mediated in part by WRKY transcription factors, in particular WRKY18, WRKY40, and WRKY60, which are induced in response to ABA and abiotic stresses (Chen et al., 2010; Pandey et al., 2010). In accordance with this, the transcriptional activation of ERF109 by high levels of light and hydrogen peroxide (H2O2) is almost completely abolished in the respective triple wrky knockout.

Not only does ERF109 gene expression become activated in response to reactive oxygen species (ROS) that result from stress stimuli; its gene product promotes ROS accumulation, which suggests that ERF109 participates in the generation of an oxidative burst (Fig. 3) (Matsuo et al., 2015). In addition, ERF109 overexpression lines show symptoms of photoinhibition and photobleaching under medium- and high-light conditions, and enhanced susceptibility to the plant pathogen Alternariabrassicae. These symptoms can be weakened by the application of antioxidants or free radical scavengers, which suggests that the constant high ROS levels in the ERF109-overexpressing plants render them more sensitive to abiotic and biotic stress. These data fit the hypothesis that ERF109 plays a role in controlling the balance of ROS (Matsuo et al., 2015). Correspondingly, erf109 knockout lines accumulate less H2O2 and ROS compared to control plants (Matsuo et al., 2015). Strikingly, although ERF108 and ERF109 appear to be strongly co-expressed over a wide set of different conditions, no elevated H2O2 and ROS were seen in ERF108 overexpression lines, which indicates that these ERFs have a distinct role in stress response.

Experimental data link ERF109 not only to stress signaling, but to developmental programs as well. Knockout plants display less lateral root primordia, whereas overexpression lines show significantly more of them. Moreover, wild-type, but not erf109 mutant roots, display an increase in the number of lateral roots following JA treatment, which suggests that ERF109 plays a role in JA-dependent initiation of lateral root development (Fig. 3). Interestingly, ERF109 overexpression lines display a number of phenotypes that resemble the overproduction of auxin, such as a long hypocotyl, and longer and more root hairs. Correspondingly, these lines contain significantly higher auxin levels, likely owing to the increased expression of the ASA1 and YUC2 auxin biosynthesis genes (Cai et al., 2014).

Apart from the control of the number of lateral roots, ERF109 activity has also been linked to radial vascular thickening through control of vascular cell division. The PHLOEM INTERCALATED WITH XYLEM (PXY) receptor is a signaling component that mediates vascular cell division, but surprisingly, the pxy knockout does not display a clear vascular cell division phenotype (Etchells et al., 2012). A transcriptomic analysis combined with genetic data revealed that the lack of such a phenotype is due to a compensatory effect through the upregulation of a number of ERF transcription factors, including ERF109. Accordingly, although both the pxy and erf109 single mutants do not display an obvious phenotype, the double mutant shows a clear reduction in vascular cell number (Fig. 3). Moreover, it has been found that vascular expression of ERF109 is controlled by ethylene signaling, which fits the observation that ethylene promotes radial growth (Etchells et al., 2012). In conclusion, although being primarily identified as a gene responsive to stress, more recent data indicate that, similar to ERF108, ERF109 might also play a role in morphogenetic changes that help to adapt to stress conditions.

ERF110

ERF110 is one of the least-studied ERFs of the subfamily and appears to be controlled by ethylene at both the transcriptional and posttranscriptional level (Fig. 3). At the gene level, its expression appears to be promoted by ethylene, whereas at the protein level, ERF110 was found to be phosphorylated and this is counteracted by ethylene signaling (Fig. 1B) (Li et al., 2012). This phosphorylation has been linked to the bolting time of the plant, as the delayed bolting phenotype of ethylene mutants can be rescued by overexpression of the wild-type ERF110 gene, but not its allele coding for a phospho-mutant (Fig. 3) (Zhu et al., 2013). Interestingly, the transcriptional activation of the above-mentioned tpoxN1 peroxidase gene by the WRAF1 and WRAF2 tobacco ERF108-like proteins upon wounding also depends on protein phosphorylation. This indicates that phosphorylation might be a general mechanism to control the activity of the X subclass of ERF transcription factors at the posttranslational level (Sasaki et al., 2002).

ERF111

ERF111, also called ABSCISIC ACID REPRESSOR 1 (ABR1), is another family member that is controlled by phosphorylation. Its phosphorylation is mediated in a Ca2+-dependent manner by the CBL9-CIPK3 module [the CALCINEURIN-B-LIKE 9 calcium-binding protein (CBL9) in complex with the CBL-interacting serine/threonine-protein kinase 3 (ClPK3)] that controls cold and ABA signal transduction (Kim et al., 2003). This observation fits with the role of ERF111 as an inhibitor of ABA responses during seed germination (Pandey et al., 2005; Sanyal et al., 2017) (Fig. 3). In addition, identical seed germination phenotypes for ABA treatment of cbl9, cipk3 and erf111 mutant plants strongly suggest that the CBL9-CIPK3 module and ERF111 operate in the same pathway. Conversely, overexpression of ERF111 results in a drought-sensitive phenotype, whereas ERF111-knockout mutants display drought tolerance (Fig. 3) (Sanyal et al., 2017).

ERF111 transcription appears to be under control of multiple transcriptional regulators, including the ABA-responsive zinc finger transcription factor Yin Yang 1 (YY1) and the multiprotein bridging factor 1 (MBF1) (Li et al., 2016; Zou et al., 2016). The latter represents a highly conserved transcriptional co-activator that regulates diverse physiological processes (Jindra et al., 2004; Liu et al., 2003). For example, the constitutive overexpression of MBF1 enhances abiotic stress tolerance, including heat and salt (Kim et al., 2007; Suzuki et al., 2008; Suzuki et al., 2005). The Arabidopsis genome encodes three MBF1 genes, and the triple knockout displays increased sensitivity to H2O2 and a significant diminution of seed germination (Arce et al., 2010). Compared to wild-type plants, ERF111 transcript levels are reduced in the triple knockout, which indicates that MBF1s regulate expression of the ERF111 gene.

ERF113

ERF113, also known as RELATED TO APETALA2.6L (RAP2.6L), is another ERF family member that is induced by salt stress and drought (Fig. 3). Additionally, ERF113 transcription is responsive to JA, salicylic acid, ABA and ethylene (Krishnaswamy et al., 2011). Correspondingly, ERF113 overexpression confers resistance to stresses that activate these hormones. For instance, overexpression of ERF113 triggers stomatal closure and enhances waterlogging tolerance (Liu et al., 2012), but it also results in a reduced germination rate. In addition to the response to hormonal cues, ERF113 activity can further be linked to developmental processes, such as shoot regeneration from root explants and ovule development (Che et al., 2006; Sun et al., 2010) (Fig. 3). Additionally, ERF113 plays a role in tissue recovery following stem incision or grafting (Asahina et al., 2011). Not only is ERF113 strongly induced after incision at the lower regions of the cut gap, but plants that express a dominant-negative allele of ERF113 also display tissue reunion defects (Asahina et al., 2011); following incision, the pith cells that surround the cut site randomly divide and elongate intrusively toward the cut surface. These responses are strongly diminished in the erf113 mutant, which suggests that ERF113 has a role in promoting cell division that is induced by wounding (Fig. 3). Expression of ERF113 at the cut site coincides with the expression of the LOX2 gene, a component of the pathway for the biosynthesis of JA. Similarly, the ERF113 gene is upregulated upon JA methyl ester administration, suggesting that JA is a primary trigger for ERF113 induction following wounding (Asahina et al., 2011).

ERF114

ERF114 is also known as ERF BUD ENHANCER (EBE) because of the observed axillary bud outgrowth upon its overexpression. Similar to ERF113, ERF114 activity has been linked with tissue regeneration (Mehrnia et al., 2013). Not only is its expression strongly induced following wounding and coincides with callus formation at the cut sites, but a further prominent feature observed for ERF114 overexpression plants is neoplasia in the form of tissue that is similar to green callus, and it is often produced at wound sites. Moreover, it has been observed that explants which overexpress ERF114 increase their rates of callus production when cultured on callus-inducing medium (Mehrnia et al., 2013). Taken together, the data indicate that ERF114 might play a role in wound healing through control of the ratio between auxin and cytokinin, which is known to be important for control of apical dominance and callus formation (Fig. 3).

ERF115

ERF115 was biochemically identified and characterized as a target of the anaphase-promoting complex/cyclosome (APC/C), which is an E3 ubiquitin ligase complex that targets cell division rate-limiting proteins, such as cyclins, for destruction (Heyman et al., 2013). Correspondingly, an ubiquitylation site was mapped at the N-terminus of ERF115 (Fig. 1B) (Walton et al., 2016). Within the plant root meristem, ERF115 expression appears to be confined to the stem cell niche (SCN) that, in Arabidopsis, is a well-organized structure. The SCN consists of a single tier of stem cells, which gives rise to the distinct tissue layers that surround a group of cells with a low proliferation rate, called the quiescent center (Heyman et al., 2014). ERF115 transcription thereby appears to specifically mark dividing quiescent center cells, because ERF115 overexpression stimulates these cells to divide. This illustrates that ERF115 is a rate-limiting factor for the proliferation of quiescent center cells that is constrained in its activity through the targeted destruction by the APC/C (Heyman et al., 2013). Strikingly, when roots are exposed to mild stress conditions, such as elevated temperatures, ERF115 is transcriptionally activated. This activation likely results in an increase in ERF115 protein abundance to a level at which it escapes the repressive action of the APC/C, triggering a round of quiescent center cell division and so generating new stem cells that replenish the older or stressed ones (Heyman et al., 2013).

Under more-severe stress settings, such as under conditions that induce DNA damage or root tip damage, ERF115 is strongly expressed in meristematic cells that are positioned immediately next to dying ones; this suggests a more general role in root tissue replenishment (Heyman et al., 2016) (Fig. 3). Upon the death of cells, the neighboring cells instantly express ERF115, which is followed by the induction of regenerative cell divisions. A putative downstream target of ERF115 is the PHYTOSULFOKINE 5 (PSK5) precursor gene which encodes a peptide hormone that was originally identified by its ability to promote proliferation of plant cells within low-density cultures (Matsubayashi and Sakagami, 1996). Thus, it appears that ERF115 is part of a mechanism that allows the replacement of damaged stem cells by new ones, thereby contributing to the reconstitution and longevity of the plant SCN (Heyman et al., 2014). Recently, ERF115 expression has been reported to be induced by salinity and to play a role in salt stress tolerance (Krishnamurthy et al., 2017); however, whether these observations are directly linked to salt-induced cell death remains to be investigated.

Control of activity of ERF by the GRAS domain transcription factor family

Recently, both ERF114 and ERF115 were found to heterodimerize with members of the GRAS-domain-containing transcription factor family (Heyman et al., 2016). GRAS transcription factors derive their name from the first three members cloned [GAI, RGA, and SCARECROW (SCR)]. The Arabidopsis genome encodes 33 members that can phylogenetically be categorized into distinct functional classes of divergent but mainly developmental processes, most of them related to stem cell and meristem organization (Bolle, 2004; Pysh et al., 1999; Tian et al., 2004). Among these, members of the SCR branch play a role in radial pattern formation within the root and shoot meristem. The LATERAL SUPPRESSOR branch controls auxillary meristem maintenance (Greb et al., 2003; Li et al., 2003; Schumacher et al., 1999), whereas HAIRY MERISTEM members prevent stem cells from differentiating (Engstrom et al., 2011; Stuurman et al., 2002; Zhou et al., 2015). Rather than controlling meristem function, members of the DELLA branch act as negative regulators of gibberellic acid signal transduction, which in turn controls a variety of developmental processes (Cao et al., 2005; Cheng et al., 2004; Dill and Sun, 2001; King et al., 2001; Lee et al., 2002; Piskurewicz and Lopez-Molina, 2009; Tyler et al., 2004).

The GRAS domain transcription factors that associate with ERF114 and ERF115 belong to the PAT1 branch, which has five members in Arabidopsis [PAT1, and the scarecrow-like proteins 1-21 (SCL1, SCL5, SCL13 and SCL21)] (Heyman et al., 2016; Torres-Galea et al., 2013). Upon their interaction, PAT1 is able to dramatically boost the regenerative capacities of ERF115, as illustrated by the spontaneous generation of callus tissue in plants co-overexpressing ERF115 and PAT1 (Heyman et al., 2016). In line with this, pat1 mutants display a reduced frequency in root tip regeneration that is similar to that of ERF115-deficient plants. PAT1 and its closest homolog SCL21 were originally identified as components that act positively on the phytochrome A (PhyA)-dependent light-signaling pathway (Bolle et al., 2000; Torres-Galea et al., 2013). PhyA predominates in dark-grown seedlings and represents the primary sensor for far-red light. Upon exposure to far-red light, PhyA is degraded; this results in the activation of the so-called de-etiolation process, which includes an inhibition of hypocotyl elongation. Similar to phyA mutants, PAT1- and SCL21-deficient plants fail to inhibit hypocotyl elongation under far-red light. Likewise, scl21 mutants display a reduced germination following a far-red light pulse (Torres-Galea et al., 2013; Torres-Galea et al., 2006). By contrast, SCL13 knockdowns display a red light-specific hypocotyl elongation phenotype, which suggests that this protein interacts with a red-light receptor, most likely phytochrome B (Torres-Galea et al., 2006). How these light phenotypes connect to the callus-inducing properties of PAT1 and SCL21 is currently unclear. Different reports have identified crosstalk networks that involve phytochrome, hormonal and abiotic stimuli, such as brassinosteroids, auxin and various stresses that result from dehydration or wounding (Auge et al., 2012; Robson et al., 2010; Sandhu et al., 2012). Cytokinins also play a role in a number of light-regulated processes, including de-etiolation (Schmülling, 2004). Accordingly, PAT1 was identified as a gene with a rapid response to cytokinin (Brenner et al., 2005). Therefore, it cannot be excluded that the observed light-responsive phenotype of the GRAS domain mutants might somehow tie in with a change in hormone balance, although more experimental data are required to solve this issue.

Through domain mapping, the motif within the ERF115 protein that is responsible for the interaction with PAT1 branch members has been pinpointed to the subfamily-specific conserved motif present in all ERF subfamily X members, with the exception of ERF112 (Fig. 2). Despite this family-specific motif, ERF114 and ERF115 appear to not be the only ERF transcription factors to heterodimerize with GRAS proteins; the DELLA protein GAI was shown to interact with the ERF transcription factor RAP2.3, and, in doing so, GAI impairs the transcriptional activity of RAP2.3 on its target promoters (Marín-de la Rosa et al., 2014). Similarly, in a study on chitin-induced transcription factors ERF5 was shown to interact with SCL13. However, the biological significance of this interaction was not analyzed (Son et al., 2012). It remains to be investigated whether the dimerization between members of the ERF and GRAS domain transcription factors is a general phenomenon, and how precisely they affect the activity of each other. Whereas ERF proteins have been shown to directly bind DNA through their AP2 domain (Ohme-Takagi and Shinshi, 1995), no such evidence is available for GRAS proteins, which, therefore, have been suggested to rather operate as transcription cofactors (Hirano et al., 2017). Moreover, both in Arabidopsis and Brassica napus, GRAS proteins have been reported to interact with histone deacetylases, which are known for their transcriptional regulation activity through histone modification (Gao et al., 2004, 2015; Zhou et al., 2005). It is therefore tempting to speculate that the ERF provides target gene specificity, whereas the GRAS interaction partner controls the regulation of its transcription by recruiting histone-modifying enzymes (Fig. 4).

Fig. 4.

Model for cooperative activity of the ERF–GRAS heterodimer. The ERF proteins accumulate in cells in response to wounding, tissue damage or cell death to form a heterodimeric complex with a GRAS transcription factor, whose expression is mainly determined by positional or tissue-dependent cues. The presence of a DNA-binding motif within the ERFs suggests that they determine target gene specificity. The GRAS factors lack DNA-binding properties, and are hypothesized to act as transcriptional co-regulators, possibly through the recruitment of histone-modifying enzymes.

Fig. 4.

Model for cooperative activity of the ERF–GRAS heterodimer. The ERF proteins accumulate in cells in response to wounding, tissue damage or cell death to form a heterodimeric complex with a GRAS transcription factor, whose expression is mainly determined by positional or tissue-dependent cues. The presence of a DNA-binding motif within the ERFs suggests that they determine target gene specificity. The GRAS factors lack DNA-binding properties, and are hypothesized to act as transcriptional co-regulators, possibly through the recruitment of histone-modifying enzymes.

Conclusions

Up to now, the subfamily X of EREB-DREB transcription factors had been mainly linked to either stress signaling or regeneration processes, but the increasing available data summarized here suggest that the members of this specific family might rather play a dual role in both of these. In doing so, these ERFs offer an elegant way to simultaneously protect injured sites and initiate their healing. Whereas ERF108 and ERF109 have been predominantly linked to JA and ABA stress signaling, data that was obtained on their tobacco orthologs suggest that they also have a role in wound repair (Sasaki et al., 2006, 2007). By contrast, whereas ERF113 and ERF115 had been demonstrated to be required for tissue repair, they have been additionally linked to JA signaling and salinity stress, respectively (Asahina et al., 2011; Krishnamurthy et al., 2017). Moreover, the fact that a target gene for ERF115 is PSK5 suggests an additional role in pathogen recognition, as plants that are defective for the PHYTOSULFOKINE RECEPTOR1 (PSKR1) display hypersensitivity toward necrotrophic fungal infection (Mosher et al., 2013). Moreover, ERF115 transcription has been found to be instantly induced in cells that surround dying cells, but whether this involves the activity of stress hormones still needs to be defined. The identification of the upstream regulators will surely help to resolve this question. Likewise, the identification of target genes for the different ERFs might help to pinpoint their relative contribution to wound protection versus repair for each of them. An intriguing question is whether the different transcription factors operate redundantly, or whether each of them can be attributed to specific wounding response and repair processes. Here, a study of the co-expression networks of the different transcription factor genes could contribute to the identification of distinct processes controlled by the various ERF–GRAS complexes. However, the final picture might be even more complex, given the posttranscriptional control of the ERFs through ubiquitylation and phosphorylation, as well as their heterodimerization with GRAS domain transcription factors (Heyman et al., 2016; Li et al., 2012; Walton et al., 2016). ERF115 binds at least two different GRAS family members, PAT1 and SCL21 (Heyman et al., 2016). It would be interesting to know whether the ERF115–PAT1 and ERF115–SCL21 complexes respond to the same upstream signals and activate the same target genes. Finally, preliminary data also suggest an interplay between at least some of the ERF subfamily X members and the WOUND INDUCED DEDIFFERENTIATION (WIND) proteins, being ERF-type transcription factors themselves (Heyman et al., 2016; Ikeuchi et al., 2017). WIND1 is rapidly induced upon tissue wounding and stimulates cells to dedifferentiate and proliferate to form callus, which precedes tissue regeneration (Iwase et al., 2011a), whereas ectopic overexpression of all four WIND family members induces callus formation (Iwase et al., 2011b). Although WIND1 was recently identified as a putative ERF115 target gene, the mechanisms controlling interplay between the different ERF subfamilies remain elusive.

Knowledge of the nature of the ERF–GRAS complexes that possess capacities to induce cell division might be important to improve transformation efficiency. Cereals have been cultivated for over 9000 years. During this period, their yield quality and quantity has been optimized through breeding. Genetic engineering tools allow further improvement of crop plants, but grasses appear to be very recalcitrant to in vitro culturing, which is an essential step during transformation techniques (Namasivayam, 2007). Most of the crop transformation protocols that are available today are of low efficiency, genotype-dependent and often work only on non-commercial low-yield cultivars. Thus, there is a need for a generic factor that can increase the in vitro culture competence of plants where this is traditionally difficult. For efficient transformation, the tissue and developmental stage of the explant is crucial: only cells that possess high cell division capacities are capable of regeneration, which explains the use of embryonic plant tissues in crop transformation protocols. Indeed, whereas in many dicotyledon plants cell division can be induced as a wounding response in leaf segments, cereal leaf segments lack the appropriate wound-healing response (Hiei et al., 2014). A recent breakthrough study reported that when the morphogenic genes WUSCHEL2 and BABYBOOM were expressed in maize, successful transformation from various explants, such as mature embryos and seedlings, was achieved in inbred maize lines that had previously been difficult to transform (Lowe et al., 2016). Transformation efficiencies that were similarly increased were also reported for rice, sorghum and sugarcane, which indicate that expressing transcription factors that control regeneration processes can make it possible to genetically modify difficult to transform monocot species and varieties (Lowe et al., 2016). Because of the involvement of ERF and GRAS family transcription factors in regeneration and developmental processes and their stem cell-inducing potential, they might be ideal candidates to improve the transformation efficiency of various crops. Further research on ERF–GRAS transcription factor interactions could shed light on mechanisms governing both plant regeneration and defense responses, and might produce valuable tools for agricultural biotechnology.

Acknowledgements

The authors thank Annick Bleys for help in preparing the manuscript and Stefanie Polyn for assistance with image design.

Footnotes

Funding

The work of our laboratories was supported by grants of the Research Foundation Flanders (Fonds Wetenschappelijk Onderzoek) (G.023616N) and the Interuniversity Attraction Poles Program (IUAP P7/29 “MARS”), initiated by the Belgian Science Policy Office (Federaal Wetenschapsbeleid). J.H. is indebted to the Research Foundation Flanders for a postdoctoral Fellowship.

References

Aida
,
M.
,
Beis
,
D.
,
Heidstra
,
R.
,
Willemsen
,
V.
,
Blilou
,
I.
,
Galinha
,
C.
,
Nussaume
,
L.
,
Noh
,
Y.-S.
,
Amasino
,
R.
and
Scheres
,
B.
(
2004
).
The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche
.
Cell
119
,
109
-
120
.
Arce
,
D. P.
,
Godoy
,
A. V.
,
Tsuda
,
K.
,
Yamazaki
,
K.-i.
,
Valle
,
E. M.
,
Iglesias
,
M. J.
,
Di Mauro
,
M. F.
and
Casalongué
,
C. A
. (
2010
).
The analysis of an Arabidopsis triple knock-down mutant reveals functions for MBF1 genes under oxidative stress conditions
.
J. Plant, Physiol.
167
,
194
-
200
.
Asahina
,
M.
,
Azuma
,
K.
,
Pitaksaringkarn
,
W.
,
Yamazaki
,
T.
,
Mitsuda
,
N.
,
Ohme-Takagi
,
M.
,
Yamaguchi
,
S.
,
Kamiya
,
Y.
,
Okada
,
K.
,
Nishimura
,
T.
, et al. 
. (
2011
).
Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion in Arabidopsis
.
Proc. Natl. Acad. Sci. USA
108
,
16128
-
16132
.
Auge
,
G. A.
,
Rugnone
,
M. L.
,
Cortés
,
L. E.
,
González
,
C. V.
,
Zarlavsky
,
G.
,
Boccalandro
,
H. E.
and
Sánchez
,
R. A.
(
2012
).
Phytochrome A increases tolerance to high evaporative demand
.
Physiol. Plant.
146
,
228
-
235
.
Baker
,
S. S.
,
Wilhelm
,
K. S.
and
Thomashow
,
M. F.
(
1994
).
The 5’-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression
.
Plant Mol. Biol.
24
,
701
-
713
.
Bolle
,
C.
(
2004
).
The role of GRAS proteins in plant signal transduction and development
.
Planta
218
,
683
-
692
.
Bolle
,
C.
,
Koncz
,
C.
and
Chua
,
N.-H.
(
2000
).
PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction
.
Genes Dev.
14
,
1269
-
1278
.
Bowman
,
J. L.
,
Smyth
,
D. R.
and
Meyerowitz
,
E. M.
(
1989
).
Genes directing flower development in Arabidopsis
.
Plant Cell
1
,
37
-
52
.
Bowman
,
J. L.
,
Smyth
,
D. R.
and
Meyerowitz
,
E. M.
(
1991
).
Genetic interactions among floral homeotic genes of Arabidopsis
.
Development
112
,
1
-
20
.
Brenner
,
W. G.
,
Romanov
,
G. A.
,
Köllmer
,
I.
,
Bürkle
,
L.
and
Schmülling
,
T.
(
2005
).
Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades
.
Plant J.
44
,
314
-
333
.
Cai
,
X.-T.
,
Xu
,
P.
,
Zhao
,
P.-X.
,
Liu
,
R.
,
Yu
,
L.-H.
and
Xiang
,
C.-B.
(
2014
).
Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation
.
Nat. Commun.
5
,
5833
.
Cao
,
D.
,
Hussain
,
A.
,
Cheng
,
H.
and
Peng
,
J.
(
2005
).
Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis
.
Planta
223
,
105
-
113
.
Che
,
P.
,
Lall
,
S.
,
Nettleton
,
D.
and
Howell
,
S. H.
(
2006
).
Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture
.
Plant Physiol.
141
,
620
-
637
.
Chen
,
H.
,
Lai
,
Z.
,
Shi
,
J.
,
Xiao
,
Y.
,
Chen
,
Z.
and
Xu
,
X.
(
2010
).
Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress
.
BMC Plant Biol.
10
,
281
.
Cheng
,
H.
,
Qin
,
L.
,
Lee
,
S.
,
Fu
,
X.
,
Richards
,
D. E.
,
Cao
,
D.
,
Luo
,
D.
,
Harberd
,
N. P.
and
Peng
,
J.
(
2004
).
Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function
.
Development
131
,
1055
-
1064
.
Dill
,
A.
and
Sun
,
T.-p.
(
2001
).
Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana
.
Genetics
159
,
777
-
785
.
Engstrom
,
E. M.
,
Andersen
,
C. M.
,
Gumulak-Smith
,
J.
,
Hu
,
J.
,
Orlova
,
E.
,
Sozzani
,
R.
and
Bowman
,
J. L.
(
2011
).
Arabidopsis homologs of the Petunia HAIRY MERISTEM gene are required for maintenance of shoot and root indeterminacy
.
Plant Physiol.
155
,
735
-
750
.
Etchells
,
J. P.
,
Provost
,
C. M.
and
Turner
,
S. R.
(
2012
).
Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling
.
PLoS Genet.
8
,
e1002997
.
Fujimoto
,
S. Y.
,
Ohta
,
M.
,
Usui
,
A.
,
Shinshi
,
H.
and
Ohme-Takagi
,
M.
(
2000
).
Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression
.
Plant Cell
12
,
393
-
404
.
Gadjev
,
I.
,
Vanderauwera
,
S.
,
Gechev
,
T. S.
,
Laloi
,
C.
,
Minkov
,
I. N.
,
Shulaev
,
V.
,
Apel
,
K.
,
Inzé
,
D.
,
Mittler
,
R.
and
Van Breusegem
,
F.
(
2006
).
Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis
.
Plant Physiol.
141
,
436
-
445
.
Gao
,
M.-j.
,
Parkin
,
I.
,
Lydiate
,
D.
and
Hannoufa
,
A.
(
2004
).
An auxin-responsive SCARECROW-like transcriptional activator interacts with histone deacetylase
.
Plant Mol. Biol.
55
,
417
-
431
.
Gao
,
M.-J.
,
Li
,
X.
,
Huang
,
J.
,
Gropp
,
G. M.
,
Gjetvaj
,
B.
,
Lindsay
,
D. L.
,
Wei
,
S.
,
Coutu
,
C.
,
Chen
,
Z.
,
Wan
,
X.-C.
et al. (
2015
).
SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme
.
Nat. Commun.
6
,
7243
.
Greb
,
T.
,
Clarenz
,
O.
,
Schäfer
,
E.
,
Müller
,
D.
,
Herrero
,
R.
,
Schmitz
,
G.
and
Theres
,
K.
(
2003
).
Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation
.
Genes Dev.
17
,
1175
-
1187
.
Guo
,
B.
,
Wei
,
Y.
,
Xu
,
R.
,
Lin
,
S.
,
Luan
,
H.
,
Lv
,
C.
,
Zhang
,
X.
,
Song
,
X.
and
Xu
,
R.
(
2016
).
Genome-wide analysis of APETALA2/Ethylene-responsive factor (AP2/ERF) gene family in barley (Hordeum vulgare L.)
.
PLoS ONE
11
,
e0161322
.
He
,
P.
,
Chintamanani
,
S.
,
Chen
,
Z.
,
Zhu
,
L.
,
Kunkel
,
B. N.
,
Alfano
,
J. R.
,
Tang
,
X.
and
Zhou
,
J.-M.
(
2004
).
Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine
.
Plant J.
37
,
589
-
602
.
Heyman
,
J.
,
Cools
,
T.
,
Vandenbussche
,
F.
,
Heyndrickx
,
K. S.
,
Van Leene
,
J.
,
Vercauteren
,
I.
,
Vanderauwera
,
S.
,
Vandepoele
,
K.
,
De Jaeger
,
G.
,
Van Der Straeten
,
D.
, et al. 
(
2013
).
ERF115 controls root quiescent center cell division and stem cell replenishment
.
Science
342
,
860
-
863
.
Heyman
,
J.
,
Kumpf
,
R. P.
and
De Veylder
,
L.
(
2014
).
A quiescent path to plant longevity
.
Trends Cell Biol.
24
,
443
-
448
.
Heyman
,
J.
,
Cools
,
T.
,
Canher
,
B.
,
Shavialenka
,
S.
,
Traas
,
J.
,
Vercauteren
,
I.
,
Van den Daele
,
H.
,
Persiau
,
G.
,
De Jaeger
,
G.
,
Sugimoto
,
K.
, et al. 
. (
2016
).
The heterodimeric transcription factor complex ERF115-PAT1 grants regeneration competence
.
Nat. Plants
2
,
16165
.
Hiei
,
Y.
,
Ishida
,
Y.
and
Komari
,
T.
(
2014
).
Progress of cereal transformation technology mediated by Agrobacterium tumefaciens
.
Front. Plant Sci.
5
,
628
.
Hirano
,
Y.
,
Nakagawa
,
M.
,
Suyama
,
T.
,
Murase
,
K.
,
Shirakawa
,
M.
,
Takayama
,
S.
,
Sun
,
T.-p.
and
Hakoshima
,
T.
(
2017
).
Structure of the SHR-SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD
.
Nat. Plants
3
,
17010
.
Hofhuis
,
H.
,
Laskowski
,
M.
,
Du
,
Y.
,
Prasad
,
K.
,
Grigg
,
S.
,
Pinon
,
V.
and
Scheres
,
B.
(
2013
).
Phyllotaxis and rhizotaxis in Arabidopsis are modified by three PLETHORA transcription factors
.
Curr. Biol.
23
,
956
-
962
.
Ikeuchi
,
M.
,
Iwase
,
A.
,
Rymen
,
B.
,
Lambolez
,
A.
,
Kojima
,
M.
,
Takebayashi
,
Y.
,
Heyman
,
J.
,
Watanabe
,
S.
,
Seo
,
M.
,
De Veylder
,
L.
, et al. 
(
2017
).
Wounding triggers callus formation via dynamic hormonal and transcriptional changes
.
Plant Physiol.
175
,
1158
-
1174
.
Ingram
,
J.
and
Bartels
,
D.
(
1996
).
The molecular basis of dehydration tolerance in plants
.
Annu. Rev. Plant Physiol. Plant Mol. Biol.
47
,
377
-
403
.
Iwase
,
A.
,
Mitsuda
,
N.
,
Koyama
,
T.
,
Hiratsu
,
K.
,
Kojima
,
M.
,
Arai
,
T.
,
Inoue
,
Y.
,
Seki
,
M.
,
Sakakibara
,
H.
and
Sugimoto
,
K.
(
2011a
).
The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis
.
Curr. Biol.
21
,
508
-
514
.
Iwase
,
A.
,
Ohme-Takagi
,
M.
and
Sugimoto
,
K.
(
2011b
).
Wind1: a key switch for plant cell dedifferentiation
.
Plant Signal Behav.
12
,
1943
-
1945
.
Jiang
,
C.
,
Iu
,
B.
and
Singh
,
J.
(
1996
).
Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus
.
Plant Mol. Biol.
30
,
679
-
684
.
Jindra
,
M.
,
Gaziova
,
I.
,
Uhlirova
,
M.
,
Okabe
,
M.
,
Hiromi
,
Y.
and
Hirose
,
S.
(
2004
).
Coactivator MBF1 preserves the redox-dependent AP-1 activity during oxidative stress in Drosophila
.
EMBO J.
23
,
3538
-
3547
.
Jofuku
,
K. D.
,
den Boer
,
B. G. W.
,
Van Montagu
,
M.
and
Okamuro
,
J. K.
(
1994
).
Control of Arabidopsis flower and seed development by the homeotic gene APETALA2
.
Plant Cell
6
,
1211
-
1225
.
Kagaya
,
Y.
and
Hattori
,
T.
(
2009
).
Arabidopsis transcription factors, RAV1 and RAV2, are regulated by touch-related stimuli in a dose-dependent and biphasic manner
.
Genes Genet. Syst.
84
,
95
-
99
.
Kagaya
,
Y.
,
Ohmiya
,
K.
and
Hattori
,
T.
(
1999
).
RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants
.
Nucleic Acids Res.
27
,
470
-
478
.
Khandelwal
,
A.
,
Elvitigala
,
T.
,
Ghosh
,
B.
and
Quatrano
,
R. S.
(
2008
).
Arabisopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor
.
Plant Physiol.
4
,
2050
-
2058
.
Kim
,
K.-N.
,
Cheong
,
Y. H.
,
Grant
,
J. J.
,
Pandey
,
G. K.
and
Luan
,
S.
(
2003
).
CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transducion in Arabidopsis
.
Plant Cell.
2
,
411
-
423
.
Kim
,
M.-J.
,
Lim
,
G.-H.
,
Kim
,
E.-S.
,
Ko
,
C.-B.
,
Yang
,
K.-Y.
,
Jeong
,
J.-A.
,
Lee
,
M.-C.
and
Kim
,
C. S.
(
2007
).
Abiotic and biotic stress tolerance in Arabidopsis overexpressing the Multiprotein bridging factor 1a (MBF1a) transcriptional coactivator gene
.
Biochem. Biophys. Res. Commun.
354
,
440
-
446
.
King
,
K. E.
,
Moritz
,
T.
and
Harberd
,
N. P.
(
2001
).
Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA
.
Genetics
159
,
767
-
776
.
Kizis
,
D.
,
Lumbreras
,
V.
and
Pagès
,
M.
(
2001
).
Role of AP2/EREBP transcription factors in gene regulation during abiotic stress
.
FEBS Lett.
498
,
187
-
189
.
Krishnamurthy
,
P.
,
Mohanty
,
B.
,
Wijaya
,
E.
,
Lee
,
D.-Y.
,
Lim
,
T.-M.
,
Lin
,
Q.
,
Xu
,
J.
,
Loh
,
C.-S.
and
Kumar
,
P. P.
(
2017
).
Transcriptomics analysis of salt stress tolerance in the roots of the mangrove Avicennia officinalis
.
Sci. Rep.
7
,
10031
.
Krishnaswamy
,
S.
,
Verma
,
S.
,
Rahman
,
M. H.
and
Kav
,
N. N. V.
(
2011
).
Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis
.
Plant Mol. Biol.
75
,
107
-
127
.
Kunst
,
L.
,
Klenz
,
J. E.
,
Martinez-Zapater
,
J.
and
Haughn
,
G. W.
(
1989
).
AP2 gene determines the identity of perianth organs in flowers of Arabidopsis thaliana
.
Plant Cell
1
,
1195
-
1208
.
Lata
,
C.
,
Mishra
,
A. K.
,
Muthamilarasan
,
M.
,
Bonthala
,
V. S.
,
Khan
,
Y.
and
Prasad
,
M.
(
2014
).
Genome-wide investigation and expression profiling of AP2/ERF transcription factor superfamily in foxtail millet (Setaria italica L.)
.
PLoS ONE
9
,
e113092
.
Lee
,
S.
,
Cheng
,
H.
,
King
,
K. E.
,
Wang
,
W.
,
He
,
Y.
,
Hussain
,
A.
,
Lo
,
J.
,
Harberd
,
N. P.
and
Peng
,
J.
(
2002
).
Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition
.
Genes Dev.
16
,
646
-
658
.
León
,
J.
,
Rojo
,
E.
and
Sánchez-Serrano
,
J. J.
(
2001
).
Wound signalling in plants
.
J. Exp. Bot.
52
,
1
-
9
.
Li
,
X.
,
Qian
,
Q.
,
Fu
,
Z.
,
Wang
,
Y.
,
Xiong
,
G.
,
Zeng
,
D.
,
Wang
,
X.
,
Liu
,
X.
,
Teng
,
S.
,
Hiroshi
,
F.
, et al. 
(
2003
).
Control of tillering in rice
.
Nature
422
,
618
-
621
.
Li
,
Y.
,
Shu
,
Y.
,
Peng
,
C.
,
Zhu
,
L.
,
Guo
,
G.
and
Li
,
N.
(
2012
).
Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism
.
Mol. Cell. Proteomics
11
,
272
-
285
.
Li
,
T.
,
Wu
,
X.-Y.
,
Li
,
H.
,
Song
,
J.-H.
and
Liu
,
J.-Y.
(
2016
).
A dual-function transcription factor, AtYY1, is a novel negative regulator of the Arabidopsis ABA response network
.
Mol. Plant
9
,
650
-
661
.
Liu
,
Q.
,
Kasuga
,
M.
,
Sakuma
,
Y.
,
Abe
,
H.
,
Miura
,
S.
,
Yamaguchi-Shinozaki
,
K.
and
Shinozaki
,
K.
(
1998
).
Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis
.
Plant Cell
10
,
1391
-
1406
.
Liu
,
Q.-X.
,
Jindra
,
M.
,
Ueda
,
H.
,
Hiromi
,
Y.
and
Hirose
,
S.
(
2003
).
Drosophila MBF1 is a co-activator for Tracheae Defective and contributes to the formation of tracheal and nervous systems
.
Development
130
,
719
-
728
.
Liu
,
P.
,
Sun
,
F.
,
Gao
,
R.
and
Dong
,
H.
(
2012
).
RAP2.6L overexpression delays waterlogging induced premature senescence by increasing stomatal closure more than antioxidant enzyme activity
.
Plant Mol. Biol.
79
,
609
-
622
.
Liu
,
S.
,
Wang
,
X.
,
Wang
,
H.
,
Xin
,
H.
,
Yang
,
X.
,
Yan
,
J.
,
Li
,
J.
,
Tran
,
L.-S.
,
Shinozaki
,
K.
,
Yamaguchi-Shinozaki
,
K.
et al. (
2013
).
Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L
.
PLoS Genet.
9
,
e1003790
.
Lowe
,
K.
,
Wu
,
E.
,
Wang
,
N.
,
Hoerster
,
G.
,
Hastings
,
C.
,
Cho
,
M.-J.
,
Scelonge
,
C.
,
Lenderts
,
B.
,
Chamberlin
,
M.
,
Cushatt
,
J.
, et al. 
(
2016
).
Morphogenic regulators Baby boom and Wuschel improve monocot transformation
.
Plant Cell
28
,
1998
-
2015
.
Marín-de la Rosa
,
N.
,
Sotillo
,
B.
,
Miskolczi
,
P.
,
Gibbs
,
D. J.
,
Vicente
,
J.
,
Carbonero
,
P.
,
Oñate-Sánchez
,
L.
,
Holdsworth
,
M. J.
,
Bhalerao
,
R.
,
Alabadí
,
D.
, et al. 
(
2014
).
Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners
.
Plant Physiol.
166
,
1022
-
1032
.
Matsubayashi
,
Y
. and
Sakagami
,
Y
. (
1996
).
Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L
.
Proc. Natl. Acad. Sci. USA
93
,
7623
-
7627
.
Matsui
,
A.
,
Ishida
,
J.
,
Morosawa
,
T.
,
Mochizuki
,
Y.
,
Kaminuma
,
E.
,
Endo
,
T. A.
,
Okamoto
,
M.
,
Nambara
,
E.
,
Nakajima
,
M.
,
Kawashima
,
M.
, et al. 
. (
2008
).
Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array
.
Plant Cell Physiol.
49
,
1135
-
1149
.
Matsuo
,
M.
,
Johnson
,
J. M.
,
Hieno
,
A.
,
Tokizawa
,
M.
,
Nomoto
,
M.
,
Tada
,
Y.
,
Godfrey
,
R.
,
Obokata
,
J.
,
Sherameti
,
I.
,
Yamamoto
,
Y. Y.
, et al. 
(
2015
).
High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots
.
Mol. Plant
8
,
1253
-
1273
.
Mehrnia
,
M.
,
Balazadeh
,
S.
,
Zanor
,
M.-I.
and
Mueller-Roeber
,
B.
(
2013
).
EBE, an AP2/ERF transcription factor highly expressed in proliferating cells, affects shoot architecture in Arabidopsis
.
Plant Physiol.
162
,
842
-
857
.
Melnyk
,
C. W.
(
2017
).
Connecting the plant vasculature to friend or foe
.
New Phytol.
213
,
1611
-
1617
.
Mitsuda
,
N.
and
Ohme-Takagi
,
M.
(
2009
).
Functional analysis of transcription factors in Arabidopsis
.
Plant Cell Physiol.
50
,
1232
-
1248
.
Mosher
,
S.
,
Seybold
,
H.
,
Rodriguez
,
P.
,
Stahl
,
M.
,
Davies
,
K. A.
,
Dayaratne
,
S.
,
Morillo
,
S. A.
,
Wierzba
,
M.
,
Favery
,
B.
,
Keller
,
H.
, et al. 
(
2013
).
The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner
.
Plant J.
73
,
469
-
482
.
Mudunkothge
,
J. S.
and
Krizek
,
B. A.
(
2012
).
Three Arabidopsis AIL/PLT genes act in combination to regulate shoot apical meristem function
.
Plant J.
71
,
108
-
121
.
Nakano
,
T.
,
Suzuki
,
K.
,
Fujimura
,
T.
and
Shinshi
,
H.
(
2006
).
Genome-wide analysis of the ERF gene family in Arabidopsis and rice
.
Plant Physiol.
140
,
411
-
432
.
Namasivayam
,
P.
(
2007
).
Acquisition of embryogenic competence during somatic embryogenesis
.
Plant Cell Tissue Organ Cult.
90
,
1
-
8
.
Nole-Wilson
,
S.
,
Tranby
,
T. L.
and
Krizek
,
B. A.
(
2005
).
AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states
.
Plant Mol. Biol.
57
,
613
-
628
.
Ohme-Takagi
,
M.
and
Shinshi
,
H.
(
1995
).
Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element
.
Plant Cell
7
,
173
-
182
.
Pandey
,
G. K.
,
Grant
,
J. J.
,
Cheong
,
Y. H.
,
Kim
,
B. G.
,
Li
,
L.
and
Luan
,
S.
(
2005
).
ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis
.
Plant Physiol.
139
,
1185
-
1193
.
Pandey
,
S. P.
,
Roccaro
,
M.
,
Schön
,
M.
,
Logemann
,
E.
and
Somssich
,
I. E.
(
2010
).
Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis
.
Plant J.
64
,
912
-
923
.
Piskurewicz
,
U.
and
Lopez-Molina
,
L.
(
2009
).
The GA-signaling repressor RGL3 represses testa rupture in response to changes in GA and ABA levels
.
Plant Signal. Behav.
4
,
63
-
65
.
Prasad
,
K.
,
Grigg
,
S. P.
,
Barkoulas
,
M.
,
Yadav
,
R. K.
,
Sanchez-Perez
,
G. F.
,
Pinon
,
V.
,
Blilou
,
I.
,
Hofhuis
,
H.
,
Dhonukshe
,
P.
,
Galinha
,
C.
, et al. 
. (
2011
).
Arabidopsis PLETHORA transcription factors control phyllotaxis
.
Curr. Biol.
21
,
1123
-
1128
.
Pysh
,
L. D.
,
Wysocka-Diller
,
J. W.
,
Camilleri
,
C.
,
Bouchez
,
D.
and
Benfey
,
P. N.
(
1999
).
The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes
.
Plant J.
18
,
111
-
119
.
Rao
,
G.
,
Sui
,
J.
,
Zeng
,
Y.
,
He
,
C.
and
Zhang
,
J.
(
2015
).
Genome-wide analysis of the AP2/ERF gene family in Salix arbutifolia
.
FEBS Open Bio.
5
,
132
-
137
.
Riaño-Pachón
,
D. M.
,
Ruzicic
,
S.
,
Dreyer
,
I.
and
Mueller-Roeber
,
B.
(
2007
).
PlnTFDB: an integrative plant transcription factor database
.
BMC Bioinformatics
8
,
42
.
Robson
,
F.
,
Okamoto
,
H.
,
Patrick
,
E.
,
Harris
,
S.-R.
,
Wasternack
,
C.
,
Brearley
,
C.
and
Turner
,
J. G.
(
2010
).
Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability
.
Plant Cell
22
,
1143
-
1160
.
Sandhu
,
K. S.
,
Hagely
,
K.
and
Neff
,
M. M.
(
2012
).
Genetic interactions between brassinosteroid-inactivating P450s and photomorphogenic photoreceptors in Arabidopsis thaliana
.
G3 (Bethesda).
2
,
1585
-
1593
.
Santuari
,
L.
,
Sanchez-Perez
,
G. F.
,
Luijten
,
M.
,
Rutjens
,
B.
,
Terpstra
,
I.
,
Berke
,
L.
,
Gorte
,
M.
,
Prasad
,
K.
,
Bao
,
D.
,
Timmermans-Hereijgers
,
J. L.
, et al. 
(
2016
).
The PLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots
.
Plant Cell
28
,
2937
-
2951
.
Sanyal
,
S. K.
,
Kanwar
,
P.
,
Yadav
,
A. K.
,
Sharma
,
C.
,
Kumar
,
A.
and
Pandey
,
G. K.
(
2017
).
Arabidopsis CBL interacting protein kinase 3 interacts with ABR1, an APETALA2 domain transcription factor, to regulate ABA responses
.
Plant Sci.
254
,
48
-
59
.
Sasaki
,
K.
,
Hiraga
,
S.
,
Ito
,
H.
,
Seo
,
S.
,
Matsui
,
H.
and
Ohashi
,
Y.
(
2002
).
A wound-inducible tobacco peroxidase gene expresses preferentially in the vascular system
.
Plant Cell Physiol.
43
,
108
-
117
.
Sasaki
,
K.
,
Ito
,
H.
,
Mitsuhara
,
I.
,
Hiraga
,
S.
,
Seo
,
S.
,
Matsui
,
H.
and
Ohashi
,
Y.
(
2006
).
A novel wound-responsive cis-element, VWRE, of the vascular system-specific expression of a tobacco peroxidase gene, tpoxN1
.
Plant Mol. Biol.
62
,
753
-
768
.
Sasaki
,
K.
,
Mitsuhara
,
I.
,
Seo
,
S.
,
Ito
,
H.
,
Matsui
,
H.
and
Ohashi
,
Y.
(
2007
).
Two novel AP2/ERF domain proteins interact with cis-element VWRE for wound-induced expression of the Tobacco tpoxN1 gene
.
Plant J.
50
,
1079
-
1092
.
Savatin
,
D. V.
,
Gramegna
,
G.
,
Modesti
,
V.
and
Cervone
,
F.
(
2014
).
Wounding in the plant tissue: the defense of a dangerous passage
.
Front Plant Sci.
5
,
470
.
Schmülling
,
T
. (
2004
).
Cytokinin
. In
Encyclopedia of Biological Chemistry
(ed.
W. J.
Lennarz
and
M. D.
Lane
), pp.
562
-
567
.
London
,
UK
:
Academic Press/Elsevier Science
.
Schumacher
,
K.
,
Schmitt
,
T.
,
Rossberg
,
M.
,
Schmitz
,
G
. and
Theres
,
K
. (
1999
).
The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family
.
Proc. Natl. Acad. Sci. USA
96
,
290
-
295
.
Sena
,
G.
,
Wang
,
X.
,
Liu
,
H.-Y.
,
Hofhuis
,
H.
and
Birnbaum
,
K. D.
(
2009
).
Organ regeneration does not require a functional stem cell niche in plants
.
Nature
457
,
1150
-
1153
.
Son
,
G. H.
,
Wan
,
J.
,
Kim
,
H. J.
,
Nguyen
,
X. C.
,
Chung
,
W. S.
,
Hong
,
J. C.
and
Stacey
,
G.
(
2012
).
Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response
.
Mol. Plant-Microbe Interact.
25
,
48
-
60
.
Stuurman
,
J.
,
Jäggi
,
F.
and
Kuhlemeier
,
C.
(
2002
).
Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells
.
Genes Dev.
16
,
2213
-
2218
.
Sun
,
S.-B.
,
Meng
,
L.-S.
,
Sun
,
X.-D.
and
Feng
,
Z.-H.
(
2010
).
Using high competent shoot apical meristems of cockscomb as explants for studying function of ASYMMETRIC LEAVES2-LIKE11 (ASL11) gene of Arabidopsis
.
Mol. Biol. Rep.
37
,
3973
-
3982
.
Suzuki
,
N.
,
Rizhsky
,
L.
,
Liang
,
H.
,
Shuman
,
J.
,
Shulaev
,
V.
and
Mittler
,
R.
(
2005
).
Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c
.
Plant Physiol.
139
,
1313
-
1322
.
Suzuki
,
N.
,
Bajad
,
S.
,
Shuman
,
J.
,
Shulaev
,
V.
and
Mittler
,
R.
(
2008
).
The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana
.
J. Biol. Chem.
283
,
9269
-
9275
.
Tian
,
C.
,
Wan
,
P.
,
Sun
,
S.
,
Li
,
J.
and
Chen
,
M.
(
2004
).
Genome-wide analysis of the GRAS gene family in rice and Arabidopsis
.
Plant Mol. Biol.
54
,
519
-
532
.
Torres-Galea
,
P.
,
Huang
,
L.-F.
,
Chua
,
N.-H.
and
Bolle
,
C.
(
2006
).
The GRAS protein SCL13 is a positive regulator of phytochrome-dependent red light signaling, but can also modulate phytochrome A responses
.
Mol. Genet. Genomics
276
,
13
-
30
.
Torres-Galea
,
P.
,
Hirtreiter
,
B.
and
Bolle
,
C.
(
2013
).
Two GRAS proteins, SCARECROW-LIKE21 and PHYTOCHROME A SIGNAL TRANSDUCTION1, function cooperatively in phytochrome A signal transduction
.
Plant Physiol.
161
,
291
-
304
.
Toufighi
,
K.
,
Brady
,
S. M.
,
Austin
,
R.
,
Ly
,
E.
and
Provart
,
N. J.
(
2005
).
The Botany Array Resource: e-Northerns, Expression Angling, and promoter analyses
.
Plant J.
43
,
153
-
163
.
Tyler
,
L.
,
Thomas
,
S. G.
,
Hu
,
J.
,
Dill
,
A.
,
Alonso
,
J. M.
,
Ecker
,
J. R.
and
Sun
,
T.-p.
(
2004
).
Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis
.
Plant Physiol.
135
,
1008
-
1019
.
Walton
,
A.
,
Stes
,
E.
,
Cybulski
,
N.
,
Van Bel
,
M.
,
Iñigo
,
S.
,
Nagels Durand
,
A.
,
Timmerman
,
E.
,
Heyman
,
J.
,
Pauwels
,
L.
,
De Veylder
,
L.
, et al. 
. (
2016
).
It's time for some “site"-seeing: novel tools to monitor the ubiquitin landscape in Arabidopsis thaliana
.
Plant Cell
28
,
6
-
16
.
Wang
,
Z.
,
Cao
,
G.
,
Wang
,
X.
,
Miao
,
J.
,
Liu
,
X.
,
Chen
,
Z.
,
Qu
,
L.-J
. and
Gu
,
H
. (
2008
).
Identification and characterization of COI1-dependent transcription factor genes involved in JA-mediated response to wounding in Arabidopsis plants
.
Plant Cell Rep.
27
,
125
-
135
.
Zhou
,
C.
,
Zhang
,
L.
,
Duan
,
J.
,
Miki
,
B.
and
Wu
,
K.
(
2005
).
HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis
.
Plant Cell
17
,
1196
-
1204
.
Zhou
,
Y.
,
Liu
,
X.
,
Engstrom
,
E. M.
,
Nimchuk
,
Z. L.
,
Pruneda-Paz
,
J. L.
,
Tarr
,
P. T.
,
Yan
,
A.
,
Kay
,
S. A.
and
Meyerowitz
,
E. M.
(
2015
).
Control of plant stem cell function by conserved interacting transcriptional regulators
.
Nature
517
,
377
-
380
.
Zhu
,
Q.
,
Zhang
,
J.
,
Gao
,
X.
,
Tong
,
J.
,
Xiao
,
L.
,
Li
,
W.
and
Zhang
,
H.
(
2010
).
The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses
.
Gene
457
,
1
-
12
.
Zhu
,
L.
,
Liu
,
D.
,
Li
,
Y.
and
Li
,
N.
(
2013
).
Functional phosphoproteomic analysis reveals that a serine-62-phosphorylated isoform of Ethylene Response Factor110 is involved in Arabidopsis bolting
.
Plant Physiol.
161
,
904
-
917
.
Zou
,
Y.
,
Chintamanani
,
S.
,
He
,
P.
,
Fukushige
,
H.
,
Yu
,
L.
,
Shao
,
M.
,
Zhu
,
L.
,
Hildebrand
,
D. F.
,
Tang
,
X.
and
Zhou
,
J.-M.
(
2016
).
A gain-of-function mutation in Msl10 triggers cell death and wound-induced hyperaccumulation of jasmonic acid in Arabidopsis
.
J. Integr. Plant Biol.
58
,
600
-
609
.

Competing interests

The authors declare no competing or financial interests.