Modulation of Class I TCP Protein Activity

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1		Ivana Viola	--	1684	2023-03-31 18:18:28	\|
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This entry is adapted from the peer-reviewed paper 10.3390/ijms24065437

TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR 1 and 2 (TCP) proteins constitute a plant-specific transcription factors family exerting effects on multiple aspects of plant development, such as germination, embryogenesis, leaf and flower morphogenesis, and pollen development, through the recruitment of other factors and the modulation of different hormonal pathways. They are divided into two main classes, I and II. The roles of class TCPs from class I in plant growth and development, as well as the modulation of their activity through interaction with other proteins and redox interconversions, proteolytic processing, or intra- or intercellular movement are discussed. Additionally, the function of these proteins in response to different environmental conditions is discussed.

Transcription factor TCP family plant development transcriptional regulation postranslational regulation

1. Introduction

Transcription factors are considered as master regulators involved in important plant responses associated with genetic reprogramming and it is well acknowledged that their activity need to be highly and finely tuned. Thus, different regulatory mechanisms such as post-translational modifications, protein-protein interactions, protein degradation or stabilization, but also protein relocalization can be considered. These interactions are highly dynamic and might affect positively or negatively the stability of transcription factors, modify their DNA binding activities and have consequences on the expression of target genes. A growing body of evidence shows the existence of a precise regulation of the activity of TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR 1 and 2 (TCP) proteins through the modulation of protein stability, DNA binding capacity and subcellular localization. For example, class I TCP protein levels are affected by proteasome-dependent degradation mechanisms ^[1]. DA1, DAR1 and DAR2 peptidases cleave TCP14, TCP15 and TCP22, leading to their inactivation and destabilization to limit cell proliferation in Arabidopsis ^[2]^[3], whereas SPINDLY (SPY) interacts with TCP14 and TCP15 preventing their proteolysis by the 26S proteasome ^[4]^[5] (Figure 1). In the absence of SPY, degradation of the TCPs is governed by interaction with F-box proteins of the KISS ME DEADLY family, negative regulators of CK signaling ^[6]. Recently, SPY was demonstrated to be an O-fucosyltransferase that modifies a number of proteins ^[7]^[8]^[9]. Inhibition of class I TCP proteolysis by SPY promotes CK responses in developing Arabidopsis leaves and flowers and the catalytic domain of SPY was identified as essential for TCP activity. However, whether SPY indeed O-fucosylates TCPs for stabilization and the mechanism by which SPY affects TCPs accumulation or stability are critical questions to answer. In addition, TCPs were identified as downstream interacting partners of mitogen-activated protein kinases (MAPKs) and PHOTOREGULATORY PROTEIN KINASES (PPKs) and evidence of direct O-GlcNAc modification and phosphorylation near the N-terminal of class I TCPs was reported ^[10]^[11]^[12]^[13]^[14]^[15]. However, the extent or roles of these modifications in the activity of TCPs are still unknown. Future studies are needed to establish the functional links between O-GlcNAcylation and phosphorylation of TCPs and plant growth regulation.

Figure 1. Scheme of the growth and developmental processes regulated by class I TCPs in Arabidopsis. The environmental conditions and interacting proteins that regulate class I TCP activity or stability are indicated. TCP-interacting proteins are shown as spheres. Green arrows and blue T-shaped lines indicate promotion and inhibition of TCP activity or stability, respectively. Red arrows and T-shaped lines indicate stimulatory and inhibitory effects by exogenous factors, respectively. The positive and negative regulatory actions of class I TCP proteins in biological processes are indicated by black arrows and T-shaped lines, respectively. For the purposes of illustration, some TCP-modulated processes are shown in one life stage, but may be operative also in other stages; see text for details.

2. Interaction with Non-TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR 1 and 2 Transcriptional Regulators

TCP proteins can function either as transcriptional activators or repressors and act through recruitment of specific non-TCP proteins by protein-protein interactions. The formation of these complexes can lead to an increase in the transcriptional activity of TCPs or exert an inhibitory or antagonistic effect, depending on the specific proteins that TCPs interact with. In some cases, a synergistic or cooperative effect on the transcriptional activity of interacting proteins was observed ^[10]^[11]^[16]^[17]^[18]^[19]^[20]^[21]^[22], in others, binding to target gene promoters is possible or enhanced by protein-protein complex formation ^[11]^[16]^[18]^[21] or, even if TCPs can bind to promoters of target genes, they function as transcriptional activators only if they interact with a partner ^[11]^[18]. On the other hand, there are protein partners that inhibit the transcriptional activity of TCPs, as for example ORANGE, ERF4 and DELLA proteins ^[23]^[24]^[25] (Figure 1). DELLA proteins interact with the DNA binding motif of TCPs, sequestering them into inactive complexes unable to bind target genes ^[23], whereas the transcriptional repressor ERF4 inhibits the ability of Arabidopsis TCP15 to activate transcription by interaction with other regions of the protein ^[24]. In addition, TCP15 acts as a working partner with ERF4 to antagonistically regulate the expression of their targets ^[24].

Although most of the class I TCP proteins have been reported as transcriptional activators, a number of reports indicate that they can also act as repressors. TCP16 and TCP21/CHE1 from Arabidopsis, PpTCP20 from peach, and GhTCP19 from cotton repress the expression of their target genes ^[26]^[27]^[28]^[29], MdTCP46 from apple blocks the binding of a transcriptional activator to its target genes, thereby negatively regulating their expression ^[30], and some TCPs interact with transcriptional repressors ^[31]. Even more, different class I TCPs can act as activators or repressors of the same target gene, as CCA1, which is activated by TCP20 and TCP22 and repressed by TCP21/CHE in Arabidopsis ^[11]^[29]. All this indicates that the vast capacity of TCPs to form complexes with different types of proteins provides a flexible mechanism to regulate growth and development in plants.

3. Class I TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR 1 and 2 Proteins in Redox Signaling

Interestingly, class I TCP transcription factor activity is regulated in a redox-dependent manner. The DNA binding capacity of class I TCPs was shown to be redox-modulated through the oxidation of a highly conserved cysteine residue localized at the beginning of helix I of the TCP domain ^[32]. Oxidizing conditions lead to the formation of an intermolecular disulfide bond between two TCP domains that would affect TCP dimer conformation, such that DNA binding and transcriptional regulation of TCP target genes is no longer possible ^[33]. This indicates that class I TCPs can act as sensors of altered redox conditions, as imbalanced H₂O₂ levels generated in response to environmental changes. Recently, a similar redox-dependent DNA interaction was reported for the only class I TCP from the liverwort Marchantia polymorpha, MpTCP1 ^[34]. Given the presence of a single conserved cysteine residue in charophycean algae and land plants, its presence might already have contributed to sensing and responding to redox changes in water-living algae and then in early diverging land plants.

Evidence has been gathered that TCPs are involved in ROS-mediated processes during stress-induced adaptive plant growth responses. For example, class I TCPs repress anthocyanin biosynthesis in Arabidopsis, but a prolonged exposure to high light intensity leads to redox inactivation of TCPs, de-repression of anthocyanin synthesis, and a protective response ^[32] (Figure 1). MpTCP1 senses ROS levels and affects the expression of several enzymes involved in ROS metabolism, mediating adaptive responses to heat stress ^[35]. In Arabidopsis, TCP9 modulates ROS homeostasis in response to nematode infection ^[36] and class I TCP double and triple mutants exhibit enhanced ROS production ^[24]. It was also reported that expression of moso bamboo PeTCP10 increases drought tolerance in transgenic Arabidopsis via ROS-regulated root growth ^[37]^[38].

In summary, several reports have indicated that class I TCPs are targets as well as modulators of changes in cellular redox homeostasis, suggesting that they may act as sensors during the response to internal and environmental conditions that affect the redox status of the cell. In this sense, it has been proposed that lower ROS levels would activate TCPs to regulate the expression of cell cycle-related genes and that JA, glutathione and TCPs might form a molecular network that controls redox regulation of the cell cycle in plants ^[39]^[40]. However, further research is needed to unravel how TCPs function, transcriptional regulation of ROS-related processes, ROS sensitivity and accumulation, and the stress-induced growth response pathways, are all connected. In addition, the effect of redox regulation of the TCPs on their interaction with non-TCP proteins, their subcellular and subnuclear localization and other post-translational modifications that may affect their activity or stability is still an open question.

4. Subcellular Distribution of Class I TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR 1 and 2 Proteins

TCP proteins were identified as nuclear proteins that can localize into substructures or subdomains in the nucleus. Interestingly, several reports indicate that nuclear distribution of TCPs differs between members and also their location is differently affected by interacting proteins. TCP14 was detected exclusively in nuclear bodies, whereas TCP8 and TCP15 homodimers were shown to localize in nuclear bodies and the nucleoplasm, respectively, in Arabidopsis ^[1]^[35]^[41]^[42]. Nuclear aggregate formation was linked to the presence of an intrinsically disordered region in the C-terminus of TCP8 ^[35] and requires an intact DNA-binding ability in TCP14 ^[1]. Interestingly, a relocation of TCP8 and TCP15 was observed upon interaction with some partners. For example, TCP8 interacts with SRFR1 in nuclear foci, but TCP8-PNM1 complexes were detected in the nucleoplasm in BiFC assays ^[41]^[43]. Furthermore, TCP8 nuclear localization seems to be affected by interaction with BZR1 ^[44]. As observed with homodimers, TCP15 was detected in the nucleoplasm when interacting with SRFR1, MYB106 and GLK1 ^[18]^[41]^[45]. However, interaction with PIF4 relocates TCP15 to nuclear speckles ^[46]. In addition, TCP19 and TCP20 mediate the localization of PRR2 in Cajal bodies and nuclear speckles ^[47], evidencing that sub-nuclear localization of TCP proteins is dependent on their interacting partners. According to the literature, accumulation of nuclear factors in distinct nuclear bodies may help to generate a high local concentration of components. This could ultimately either enhance or decrease the biological function of such proteins. This sub-nuclear compartmentalization process might also contribute to modifying protein behavior and to the regulation of their stability or activity. In this sense, TCP14 nuclear bodies are recruited to JAZ3-degradation bodies by the effector protein HopBB1 from Pseudomonas syringae ^[1]. In addition, TCP8, TCP14 and TCP15 are redistributed into nuclear foci or speckles when bound to the SUMO conjugation enzyme SCE1, suggesting that these TCP foci are sites for SUMO conjugation of TCPs ^[42]. A recent discovery indicates that TCP1 from Marchantia polymorpha (MpTCP1) acts as a transcriptional repressor through its ability to form protein speckles in the nucleus and thereby physically block access to the chromatin ^[48]. The nature of these subnuclear localizations has yet to be explored, but could be sites of suppression, enhanced activation, or both, at multiple genetic loci. As also mentioned above, recruitment to specific sites may be involved in the degradation or post-translational modification of the TCPs. Future work should focus on the conditions or factors that modulate the sub-nuclear localization patterns of class I TCP members and the biological relevance of the formation of these TCP-containing nuclear bodies. In addition, although TCPs are primarily detected in the nucleus, different localizations of TCP-containing protein-protein complexes were observed depending on environmental conditions ^[49]. These reports evidence an additional level of TCP activity modulation depending not only on their interacting partners but also on cellular or environmental conditions.

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Subjects: Biochemistry & Molecular Biology

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Ivana L. Viola

Antonela L. Alem

Rocío M. Jure

Daniel H. Gonzalez

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Update Date: 03 Apr 2023

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