Abstract
The complex plant body is created by means of an elaborate system that dictates the differentiation of cells with distinctive features as well as proper growth and development. We have reviewed the literature-reported experimental evidence for post-translational modifications (PTM)s that modulate plant differentiation. We found that phosphorylation, ubiquitination, glycosylation, acetylation, and methylation are associated with plant differentiation. Phosphorylation mediated by MAPK within cytoplasm and nucleus facilitates plant differentiation. Convergence between phosphorylation, ubiquitination, and deacetylation is displayed in transcription repressor complexes modulating stem daughter, germ cell, and leaf differentiation. Reversible phosphorylation and deubiquitination made the phosphorylation and ubiquitination of PIN auxin transporters which supported the precise PIN-mediated auxin transport dynamic. The participation of several PTM types during plant cell differentiation suggests a new layer in the plant cell differentiation process. Efforts to develop deep mass spectrometry-based PTM identification could facilitate deciphering the interconnection of the variety of PTMs in this field.
Key message
Comprehensive revision of post-translational modifications associated with plant differentiation yields several post-translational modifications linked with molecular and cellular mechanisms modulating plant cell differentiation. Post-translational modification-enrichment coupled to advanced proteomics provide the resource for further discovery in this plant differentiation new layer.
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Introduction
Understanding plant cell differentiation requires knowledge of molecular and cellular mechanisms that control protein function. Much work has focused on investigating the function of proteins that govern differentiation at early embryo development, as well as the development of meristem cells, phloem, xylem, and the root system. However, proteins are dynamically regulated during differentiation and require the coordination of the over thirty cell types and the variety of tissues present in the plant body (Lyndon 1990; Niklas and Kutschera 2010; Ohtani et al. 2017). Posttranslational modifications (PTM)s have emerged as a crucial mechanism to modulate gene expression, chromatin remodeling events, and synthesis and transport of promoter growth regulators (PGR)s. Small molecules such as auxins and cytokinins are PGRs, which significantly influence plant development.
PTM types present in proteins have been accumulated so far. Massive detection has been made possible with advances in LC–MS/MS and improved protein databases by RNA-seq technologies. Here, we have been surveyed and discussed the literature-reported experimental evidence for PTMs affecting plant differentiation, mainly PTM types deposited in the Swiss-Prot database (Khoury et al. 2011). Some of the PTMs have been shown to affect plant differentiation. They can alter either molecular components such as transcription factor such as SHR and TOM7, protein–protein interactions within protein complexes responsible of regulating the gene expression, turnover of key proteins during cell fate such as E2F, DBP, and SHR, or modulate cell events such as cell enlargement and cell wall remodeling, thus accomplishing PTMs essential for plant differentiation (Fig. 1). In particular, phosphorylation is essential in auxin transport mediated by PINs. Ubiquitination is known as essential for protein turnover. However, new additional functions have described in plants that are also linked to plant differentiation, such as histone H2B monoubiquitination responsible for regulating the gene expression.
Post-translational modifications
In addition to the protein processing by cleavage with proteases or the modification of the side chain of amino acid residues by oxidation, proteins contain residues with attached chemical groups or peptides (Wang et al. 2014). The chemical groups and related processes include the phosphorylation of Ser, Thr or Tyr residues; acetylation of Lys residues; glycosylation of Asp residues to produce N-glycans and Ser/Thr residues to produce O-glycans; lipidation of Cys, Ser, and Gly residues; and AMPylation of Ser, Thr or Tyr residues. Peptide attachment to amino acid residues includes ubiquitination and ubiquitin-like attachment. Ubiquitination of the Lys residues produces monoubiquitination, poly-monoubiquitination, and poly-ubiquitination. Some of those PTMs are unknown in plant differentiation, including AMPylation, palmitoylation, and farnesylation. Also, participating PTMs such as nitration, sumoylation, and autophagy in plant differentiation is suggested from the genetic analysis of writer enzymes. We think they can sustain new molecular mechanisms, but protein targets are unknown. Recent studies have been increased our catalog of proteins with PTM associated to plant cell or tissue undergoing differentiation (Table 1). Protein classes associated with the lipid metabolism, fatty acid pathway, ribosomal proteins, autophagy-mediated mitochondria degradation, and plant cell death are of particular interest. We anticipate the need to undertake further investigation.
Protein activation, localization, and stability, as well as protein–protein interactions are major effects on the addition of PTM to protein factor commonly associated with plant differentiation (Table 2). (PIN)-dependent auxin transport and cell cycle progression are a cellular mechanism where phosphorylation and ubiquitination have converged. The biological function of PTM is mediated by writer, eraser, and reader proteins, responsible for adding, removing or recognizing the PTM, correctly (Fig. 1). Writer enzymes include ubiquitin ligases, kinases, and glycosyltransferases, whereas eraser enzymes include phosphatases, glycosidases, and histone deacetylases. Regulation of gene expression by histone modifications with acetylation or methylation, alteration of localization of transcription factors and kinases within cytoplasm and nucleus, degradation of transcription factors into the 26S proteoasome, and protein–protein interactions that modulate the expression of genes of the cell cycle and genes associated to the differentiation are the main molecular mechanisms emerging to promote differentiation.
PTMs in the cell cycle
Molecular events modulating the cell cycle and endoreplication that are linked to PTMs include the phosphorylation of retinoblastoma-related (RBR) protein, the activation and degradation of the transcription factors E2 Factor (E2F)s and E2F-like DPBs as well as CDKs (cyclin-dependent protein kinases) (Bhosale et al. 2019; del Pozo et al. 2002; Ebel et al. 2004; Gutierrez et al. 2002; Inzé and De Veylder 2006). The writer enzymes CDKA-CycD3;1 phosphorylate RBR, thus releasing RBR from the protein complex RBR-E2F-DBP (Menges et al. 2006; Nakagami et al. 2002) (Fig. 2). Furthermore, E2F-DBP promotes the expression of a variety of genes with a role in cell cycle progression and endoreplication (Müller et al. 2001; Wang et al. 2018b). Epigenetic reprogramming is required for cell cycle progression, via methylation of histone-Lys residues H3K4me3 (Pinon et al. 2017). Decreasing phosphorylated RBR amount correlates with the inhibition of the cell cycle progression and pavement cell differentiation (Ahn et al. 2016). A writer complex based in the ubiquitin ligase SCFSKP2A directs the ubiquitination of DBP and E2F, but DBP requires phosphorylation to become a ubiquitination substrate (del Pozo et al. 2002, 2006). Writer enzyme phosphorylating DBP before ubiquitination is unknown but could be a CDKA/CycA complex as in humans.
PTMs in the nuclei
The proteins’ PTM state may elicit a cell’s shift to a differentiated state. Evidence for cellular protein re-localization upon the addition of PTM is currently emerging. In the stomatal differentiation, polarization of the membrane-associated BASL, a non-membrane integral protein, is tightly regulated by MPK6-dependent phosphorylation. With the specific localization, BASL can distinguish two daughter cells derived from the asymmetric stomatal division. BASL is polarized to the large cell, where it promotes the migration of MPK3 and MPK6 in the nucleus, promoting phosphorylation and destabilization of the transcription factor SPCH, thus differentiating the two daughter cells (Zhang et al. 2016). MAPK-dependent phosphorylation in the nucleus was surprising since most of our knowledge is associated with its role in the cytoplasm. Researchers suggest that vesicular trafficking may be involved in BASL polarity (Lampard et al. 2008; Zhang et al. 2016). Very recent research shows a link between ligand-receptor interaction and the active state of transcription factor SPCH. This signaling implicates the action of cytokinin on the signaling peptide EPF1 and its receptor ERL1 (reviewed in Qi et al. 2017; Vatén et al. 2018; Zoulias et al. 2018). MAPK-dependent modulating pathways are an emerging theme in the field of differentiation (reviewed in Bigeard and Hirt 2018; Krysan and Colcombet 2018). Therefore, we anticipate that the determination of nucleus MAPK targets may become one of the most important developments in the field, taking advantage of the recent advances in the phosphopeptide enrichment strategies.
Genetic and biochemical studies highlight the participation of transcription repressor complexes during the differentiation of cells. Eraser enzymes such as the histone deacetylases that include HDAC6, HDAC18, HDAC19, and HDAC101 are recruited through accessory co-repressors by transcription factors to modulate the acetylation of histones (Chen et al. 2019; Li et al. 2015; Liu et al. 2013; Yang et al. 2016a). Transcription factors targeting genes associated to stem daughter, germ cell and leaf differentiation that recruit the co-repressor TPL/TPR include WOX5, SPL and TIE1; these repressing complexes require HDAC19 (Pi et al. 2015; Zhang et al. 2015) (Fig. 3). Endosperm cell differentiation utilizes co-repressors NFC103/MSI1 and SNL1/SIN3-like (Yang et al. 2016a). Hyperacetylation of histones is associated with the expression of multiple genes involved in differentiation, which include transcription factors with the ability to drive a rapid configuration to the differentiation state since they target a group of genes. Evidence for the participation of ubiquitination modulating the transcription repressor complexes is emerging (Zhang et al. 2017). Further investigation will need to find ubiquitin ligases responsible for ubiquitinating SPL and which signals can trigger the MPK3/6-dependent phosphorylation to increase the stability of SPL (Fig. 3A). WOX5-dependent differentiation in the root requires the ubiquitin ligase DWDPRL1, which calls for the implementation of enrichment of ubiquitinated proteins or peptides containing the ubiquitinated site to identify targets of this ubiquitin ligase (Fig. 3B). Identifying cell signals promoting the degradation of TIE1 in the leaf under differentiation will also be important.
Analysis of reversible acetylation associated with the transcription repressor complexes reveals two sites for H3 (K9 and K14) and four sites for H4 (K5, K8, K12, K16). Among those sites, H3K14ac and H4K5ac are the most frequent. The transcription repressor complex based in GEM that modulates the acetylation and methylation status of histones (Caro et al. 2007), the histone acetyltransferase writer enzymes, and the histone lysine methyltransferases have been shown to drive transcriptional repression during differentiation or maintenance of stem cells (Rodríguez-Sanz et al. 2014).
Ontogeny analysis of plant cells has revealed that writer enzyme kinases and eraser enzyme phosphatases modulate cell division type and are required during cell differentiation. By limiting the progressive dephosphorylation of CDKA;1, the antiphosphatase PAS2 inhibits the cell cycle progression and dictates which cells are committed to differentiation (Da Costa et al. 2006). Negative regulators are required in the cell division plane orientation and periclinal and asymmetrical cell division during vascular cell, stomatal cell, and guard cell differentiation (Cruz-Ramírez et al. 2012; Han and Torii 2019; Houbaert et al. 2018; Matos et al. 2014). Most of the work has focused on transcription factors that mediate the repression of CDKs, either directly stopping cell division (i.e. FAMA-mediated repression of CDKB1;1), or indirectly by the induction of repressors by which a constraint in the expression of CDKs is established (i.e. MUTE-mediated induction of CDKB1;1 CDKB2;1, CDC5;1, and CDKB1 repressors such as FLP and FAMA) (Umeda et al. 2019).
Genetic and proteomic studies on tissues undergoing differentiation, including cotton fiber, wood formation, and root differentiation, have revealed intense participation of writer and eraser enzymes that modulate the glycosylation and phosphorylation of proteins and methylation of histones. The writer enzyme DGL1 and the eraser enzyme GCS1 responsible for the N-linked glycosylation of proteins and N-glycan precursor trimming, respectively (Boisson et al. 2001; Lerouxel et al. 2005). Likewise, the delivery of free N-glycans by glycanases is emerging as a relevant theme in the field (Maeda and Kimura 2014; Veit et al. 2018). Impairment of those enzymes in vivo is associated with defects in the differentiation of the central root cylinder, and cell enlargement. Cell wall integral proteins are the target of glycosylation during cotton fiber differentiation (Kumar et al. 2013). Three methylation sites of histones H3K4me3 are targeted during wood formation to transcriptional regulation of enzymes that include cellulose and xylan biosynthesis (Hussey et al. 2015).
Precise polar auxin transport
Pin-formed (PIN)-dependent auxin transport is one of the most studied mechanisms associated with the cell’s transition to a differentiation state. Writer enzymes D6PK and PID drive the specific phosphorylation of conserved Ser in cytoplasmic loop regions of PIN1 and PIN3 (Fig. 4a) (Zourelidou et al. 2014). To switch the direction of the PIN-dependent auxin transport, plants use eraser enzymes that include PP2A phosphatase for reversible phosphorylation of PIN1 (Fig. 4b) (Michniewicz et al. 2007). Determining the targets of this eraser enzyme is very promising since its homolog in mammals modulates conserved pathways such as mTOR signaling, MAPK signaling, and RBR phosphorylation. It is also unknown if the methylated form of PP2A complex participates in specifying phosphorylated sites of PINs for reversible phosphorylation or whether the interaction of PP2A catalytic subunit with TAP46 which regulates autophagy and nutrient recycling is also involved in PIN-dependent auxin transport. Additional rapid redistribution of the auxin gradient is mediated by ubiquitination. Over 17 Lys residues of PIN2 serve as sites for ubiquitination with the K63-linked ubiquitin chain and target the PIN2 to endocytic sorting and vacuolar degradation (Leitner et al. 2012). The identity of the ubiquitin ligase targeting PIN2 ubiquitination and the participating DUBs, which should rescue PIN2-ubiquitin conjugates, is unknown. Some of those ubiquitination sites are thought to be conserved in PIN1, PIN3, PIN4, and PIN7, but they need to be tested (Fig. 4a).
PTMs associated with loss of differentiation
The loss of differentiation is the result of cell death of the conducting cells of the xylem (tracheary elements) or nucleus removal from the conducting cells of the phloem (sieve elements) (Blob et al. 2018; Schuetz et al. 2013). A pathogen attack by Verticillium longisporum on Arabidopsis leaves, hypocotyls, and roots produces the transdifferentiation of parenchyma cells to xylem cells. The phenomena of xylem hyperplasia are, in part, explained by the transcription factor VND7 (Reusche et al. 2012). Moreover, a comparative proteomic study using Verticillium dahliae and an autophagy depletion system by the atg10-1 mutant reveals that xylem hyperplasia is correlated with an increase of lignification that may act in concert with autophagy bodies to clear vascular pathogens (Wang et al. 2018a).
Transcription factor movement is mediated by PTMs
Analysis of predictable phosphorylation sites and protein movement of proteins, most of them annotated as transcription factors, have revealed that protein–protein interactions and phosphorylation are responsible for protein movement to execute differentiation. Transgenic lines expressing modified SHR at the predictable phosphorylation site T289 by replacement of T by I display an impaired ability to import SHR into the nucleus, while the substitution in CPC at W76A reduces the nuclear localization (Gallagher et al. 2004; Kurata et al. 2005). S39 and S42 are predictable phosphorylation sites of TMO7, and their replacement by S39A and S42A hampers intracellular movement (Lu et al. 2018).
Concluding remarks and future perspectives
Plant cell differentiation implies a hierarchical organization of plant cells and tissues. The acquisition of distinctive features of plant body cells by the differentiation process is accompanied by multiple morphological changes and modulation of the expression of genes with a variety of functional identities. Although the studies cited in this work present evidence for modulation of differentiation in plant cells at the protein level, our knowledge of how PTMs drive differentiation among the variety of cells and tissues is still emerging. We note PTMs as an additional layer in the plant cell differentiation process. Recent studies show the participation of phosphorylation, reversible acetylation, ubiquitination, and glycosylation of proteins with a role in the differentiation process by auxin transport, epigenetic regulation of gene expression, and protein degradation. One of the next challenges in the field will consist in deciphering the dynamic of PTM-types and the interconnection of the target proteins during the plant cell differentiation that takes place from early embryo development to the conception of the mature plant. Additional challenges to PTM analysis during differentiation will come from the existence of multiple sites for a PTM, the broad range of PTMs that can co-exist in a target protein, and the dynamic nature of PTMs introduced by the action of eraser enzymes in the cell. The development of new tools that can dissect homogeneous specific cell and tissue type samples in addition to the current protocols could enable significant advances (Endo et al. 2016).
The primary function of phosphorylation is the activation/de-activation of enzymes; recent studies show that phosphorylation alters protein–protein interactions and intracellular localization. Phosphorylation is a prevailing modification among PTMs with a role in plant cell differentiation. Notably, phosphorylation is determined by intracellular specialization by the polar localization of the active kinase complex in the nucleus. Determining new MAPK targets in the nuclei will be of particular importance to get insight into plant cell differentiation, where protocols for specific isolation of nuclei, phosphopeptide enrichment, isobaric peptide labelling (TMT, iTRAQ), 15 N metabolic labelling of proteins, and the LC–MS/MS technology will be essential.
Ubiquitination alters protein features from stability to localization. Our knowledge of the ubiquitination of proteins with a role in plant cell differentiation is limited to a few targets. These targets include RBR interacting proteins, mono-ubiquitination of H2B, and polyubiquitination of PIN1 and PIN2. The understanding of the action of multiple PTMs on proteins with a role in plant cell differentiation, as well as the action of eraser enzymes that remove PTMs from targets, is emerging. Recent studies show the participation of phosphatases including PP2A and deacetylases including HDA19 in the differentiation process.
Because the PTMs of proteins support cell cycle transition, plastid division, cell wall organization, the transport of a variety of PGRs and cell signaling in an array of intracellular environments during plant cell differentiation, our understanding of the concerted action of PTMs will contribute to deciphering how the plant constructs the plant body and how this knowledge can be used to improve agricultural traits.
Abbreviations
- SHR:
-
Shortroot
- TOM7:
-
Target of monopteros7
- E2F:
-
E2 factor
- DPB:
-
DP‐related genes
- CDKA:
-
Cyclin-dependent kinase A
- CycD3:
-
Cyclin-D3
- SCF:
-
SKP1-CUL1-F-box
- SKP2A:
-
S-Phase kinase-associated protein 2A
- BASL:
-
Breaking of asymmetry in the stomatal lineage
- SPCH:
-
Speechless
- EPF1:
-
Epidermal patterning factor1
- ERL1:
-
Erecta-Like1
- HDAC:
-
Histone deacetylase
- TPL/TPR:
-
Corepressors recruitment of topless/topless-related
- WOX5:
-
Wuschel5
- SPL:
-
Sporocytless
- TIE1:
-
TPC Interactor containing EAR Motif Protein1
- NFC103/MSI1:
-
MSI type nucleosome/chromatin assembly factor C/ Multicopy Suppressor of Ira1
- SNL1/SIN3-like:
-
Swi-Independent3-Like1/Swi-Independent3-Like1
- GEM:
-
GL2 expression modulator
- PAS2:
-
Antiphosphatase Pasticcino2
- DGL1:
-
Defective glycosylation1
- GCS1:
-
α-Glucosidase1
- mTOR:
-
Mammalian target of rapamycin
- PP2A:
-
Protein phosphatase 2A
- TAP46:
-
2A Phosphatase associated Protein46
- DUB:
-
Deubiquitinating enzymes
- VND7:
-
Vascular-related NAC Domain7
- TMT:
-
Tandem mass tag
- iTRAQ:
-
Isobaric tag for relative and absolute quantitation
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This work was supported by the National Council of Science and Technology (FS-1515 to Víctor M. Loyola-Vargas).
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Aguilar-Hernández, V., Brito-Argáez, L., Galaz-Ávalos, R.M. et al. Post-translational modifications drive plant cell differentiation. Plant Cell Tiss Organ Cult 143, 1–12 (2020). https://doi.org/10.1007/s11240-020-01908-0
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DOI: https://doi.org/10.1007/s11240-020-01908-0