Skip to main content

Advertisement

Genome-scale analysis of regulatory protein acetylation enzymes from photosynthetic eukaryotes

BMC Genomics volume 18, Article number: 514 (2017) | Download Citation

Article metrics

Abstract

Background

Reversible protein acetylation occurring on Lys-Ne has emerged as a key regulatory post-translational modification in eukaryotes. It is mediated by two groups of enzymes: lysine acetyltransferases (KATs) and lysine deacetylases (KDACs) that catalyze the addition and removal of acetyl groups from target proteins. Estimates indicate that protein acetylation is second to protein phosphorylation in abundance, with thousands of acetylated sites now identified in different subcellular compartments. Considering the important regulatory role of protein phosphorylation, elucidating the diversity of KATs and KDACs across photosynthetic eukaryotes is essential in furthering our understanding of the impact of reversible protein acetylation on plant cell processes.

Results

We report a genome-scale analysis of lysine acetyltransferase (KAT)- and lysine deacetylase (KDAC)-families from 53 photosynthetic eukaryotes. KAT and KDAC orthologs were identified in sequenced genomes ranging from glaucophytes and algae to land plants and then analyzed for evolutionary relationships. Based on consensus molecular phylogenetic and subcellular localization data we found new sub-classes of enzymes in established KAT- and KDAC-families. Specifically, we identified a non-photosynthetic origin of the HD-tuin family KDACs, a new monocot-specific Class I HDA-family sub-class, and a phylogenetically distinct Class II algal/heterokont sub-class which maintains an ankyrin domain not conserved in land plant Class II KDACs. Protein structure analysis showed that HDA- and SRT-KDACs exist as bare catalytic subunits with highly conserved median protein length, while all KATs maintained auxiliary domains, with CBP- and TAFII250-KATs displaying protein domain gain and loss over the course of photosynthetic eukaryote evolution in addition to variable protein length. Lastly, promoter element enrichment analyses across species revealed conserved cis-regulatory sequences that support KAT and KDAC involvement in the regulation of plant development, cold/drought stress response, as well as cellular processes such as the circadian clock.

Conclusions

Our results reveal new evolutionary, structural, and biological insights into the KAT- and KDAC-families of photosynthetic eukaryotes, including evolutionary parallels to protein kinases and protein phosphatases. Further, we provide a comprehensive annotation framework through our extensive phylogenetic analysis, from which future research investigating aspects of protein acetylation in plants can use to position new findings in a broader context.

Background

Reversible protein acetylation of Lys-Nε is now recognized as a key regulatory post-translational modification in eukaryotic organisms, including H. sapiens [1], D. melanogaster [2], S. cerevisiae [3] and A. thaliana [4, 5]. Reversible protein acetylation is mediated by two groups of enzymes: lysine acetyltransferases (KATs) and lysine deacetylases (KDACs), which catalyze the addition and removal of acetyl groups from target proteins. Estimates indicate that protein acetylation is second to protein phosphorylation in abundance, with thousands of sites now identified in multiple subcellular compartments [6, 7].

All known eukaryotic genomes encode at least four families of KATs (MOZ, YBF2, SAS2, and TIP60 (MYST); GCN5/PCAF-related N-acetyltransferases (GNAT); p300/CREB binding protein (CBP); TATA binding protein-associated factors (TAFII250)) and two families of KDACs (histone deacetylase (HDA/RPD3); sirtuin (SRT)), while land plants maintain an additional family of KDACs (HD2-tuin (HDT)). Those KAT and KDAC proteins which have been characterized have been found to be primarily localized to the nucleus and cytosol [8,9,10,11], with some SRT-KDACs targeted to the mitochondria [12]. Some KDACs have also shown stimuli-dependent movement between compartments [8], which likely contributes to the diversity of subcellular compartments and protein targets for regulatory acetylation events.

In photosynthetic eukaryotes most research examining reversible protein acetylation and the corresponding KATs and KDACs has been conducted in Arabidopsis thaliana (Arabidopsis) [4, 5]. However, with the increased availability of sequenced genomes, analysis of protein acetylation in crop plants such as rice [13, 14], soybean [15] and grape [16] amongst others [17, 18] has been conducted. KATs and KDACs have been implicated in a number of regulatory functions. MYST-family proteins have roles in seed [19] and gametophyte [20] development as well as flowering [21], while GNAT-family proteins function in plant immunity [22], hormone signaling [23] and light signaling [24]. Less is known about the function of CBP- and TAFII250-family KATs in photosynthetic eukaryotes. CBP KATs are involved in the regulation of flowering [25], sugar responses [26] and ethylene signaling [27], while TAFII250 KATs have so far only been implicated in seed development [28]. Similarly, many KDACs have also been examined. HDA KDACs have been implicated in regulating flowering [29], gametophyte development [30], light signaling [31], cell differentiation [32, 33], seed maturation [34] and hormone signaling [35]. SRT-family proteins participate in the regulation of mitochondrial energy metabolism and metabolite transport [12], while the function of HDT-family KDACs remains largely unknown [36].

Despite an expanding volume of research investigating the roles of KDACs and KATs in photosynthetic eukaryotes, a multi-genome scale comparison is still lacking. Multi-genome scale analyses are useful in drawing molecular evolutionary connections between organisms and developing new hypotheses for protein family evolution. While molecular research is underway in photosynthetic eukaryotes ranging from algae for biofuel production [37] to rice for nutritional enhancement [38], comparative genome scale analyses provide new fundamental insights into the evolution of eukaryotic genomes and can help to discover new, conserved targets for biotechnology. The genome-scale molecular phylogenetic analysis of regulatory protein acetylation enzymes we report here demonstrates how these enzyme families have evolved in photosynthetic eukaryotes. We have found considerable changes in encoded protein complements, subcellular localization as well as protein domain organization and structure. We also identified new and unique algae-specific enzyme classes and sub-classes. Together, we have built a compendium of protein acetylation enzymes from sequenced photosynthetic eukaryotes utilizing accepted non-photosynthetic eukaryote gene and protein nomenclature to establish a clear family, class and sub-class annotation structure for photosynthetic eukaryotes.

Results

Prevalence of reversible protein acetylation enzymes differs in photosynthetic eukaryotes

Based on publically available genome resources, KDAC and KAT protein orthologs were isolated from 53 sequenced photosynthetic eukaryotes (see material and methods). Consistent with non-photosynthetic eukaryotes, we identified two KDAC and four KAT families, in addition to the previously identified plant-specific HDT KDAC-family (Fig. 1). KDAC and KAT family sizes were generally similar in land plants and comparable between monocots and dicots (Additional file 1). However, we found gene expansions and losses of specific families/members over evolutionary time. For example, monocots possessed higher average HDA, HDT and CBP protein numbers than dicots, while early land plants S. moellendorfii and P. patens maintained fewer HDA, HDT and CBP proteins but an increase in SRT and GNAT family sizes (Additional file 1).

Fig. 1
figure1

Prevalence of reversible lysine deacetylase (KDAC) and acetyltransferase (KAT) machinery across photosynthetic eukaryotes. Depicted are the histone deacetylase/reduced potassium deficiency 3 (HDA/RPD3; Light Blue), HD-tuin (HDT; Dark Blue) and sirtuin (SRT; Purple) KDACs as well as GCN5-related n-terminal acetyltransferases (GNAT; Green), MOZ, Ybf2, Sas2 and Tip60 (MYST; orange), p300/CREB binding protein (CBP; brown) and TATA binding protein associated factors (TAFII250; Red) acetyltransferases. The taxonomic tree was constructed using phyloT as outlined in the Materials and Methods. Each number corresponds to the number of genes encoded by that organism for the given KDAC or KAT family

Full size image

In addition of the differences in higher plants, algae genomes have an elevated diversity in both KDAC and KAT families (Fig. 1). We found that green, red and brown algae all lack HDT KDACs, while red algae also lack CBP KATs. Furthermore, 33% of red algae exclusively maintain only HDA KDACs and GNAT KATs. Consistent with red algae, the glaucophyte C. paradoxa lacks CBP KATs, and consistent with all other algae, C. paradoxa also lacks HDT KDACs.

When we compared all photosynthetic eukaryote KDACs and KATs with representative orthologs of non-photosynthetic organisms, we discovered significant changes in the number of reversible protein acetylation enzymes in the kingdom Plantae (Additional file 2: Figure S1); most changes can be found among KDACs, fewer among the KATs (Additional file 2: Figure S1). HDA and HDT KDACs of both monocots and dicots have significantly expanded families, while the SRT KDACs are significantly contracted (Additional file 2: Figure S1). Similarly, monocot and dicot KDAC families also have a significant expansion (Kruskal-Wallis Test pval < 0.05) in HDA and HDT family sizes relative to algae (Additional file 2: Figure S2). This expansion is mirrored in the CBP-family KATs, the only KAT family that maintains a significant difference in family size with an increase in monocot and dicots relative to representative non-photosynthetic eukaryotes (Additional file 2: Figure S1). Further comparisons of photosynthetic eukaryotes revealed significant changes amongst CBP and TAFII250 KATs between algae and land plants, with both monocots and dicots maintaining increased family sizes (Additional file 2: Figure S3).

Orthologous reversible protein acetylation enzymes in photosynthetic and non-photosynthetic eukaryotes have variable domain architecture

Given that the presence or absence of domains can determine protein function, we investigated the domain makeup of each KDAC and KAT family. We compared median protein size (Figs. 2 and 3, black horizontal bars), protein domain localization and protein domain distribution (Figs. 2 and 3, histograms in color; see materials and methods) for each KDAC and KAT family. With protein number and size distribution not necessarily normally distributed, median protein length was used. In photosynthetic eukaryotes protein length variation was limited for all KDAC families except the HDT KDACs (Fig. 2) while protein length was variable for 2 families of KATs; CBP and TAFII250 (Fig. 3). CBP KAT median protein length increased from green algae to dicots, while TAFII250 KATs have a variable median protein length (Fig. 3). When compared to non-photosynthetic eukaryote orthologs, median protein length of each KDAC and KAT family was comparable, with the exception of monocot CBP and TAFII250 KATs, glaucophyte/red algal TAFII250 KATs, as well as green algal and heterokont CBP KATs (Figs. 2 and 3).

Fig. 2
figure2

Protein sizes and functional domains of photosynthetic eukaryotic KDACs: a) HDA-Family Deacetylases, b) SRT-Family Deacetylases and c) HDT-Family Deacetylases. Each KDAC family was divided by species type. These divisions include: dicot, monocot, green algae, red algae/glaucophytes, heterokont/other photosynthetic eukaryotes (cryptophytes & haptophytes) and non-photosynthetic eukaryotes. Horizontal black bars depict median protein length within a given species-type for a given KDAC-family. Protein domains are depicted by colored histograms (x-axis: relative positional distribution of protein domains per depicted class of proteins, y-axis: prevalence of domain across the class of proteins). Domain information was derived from PFAM and ProSITE (Additional file 3)

Full size image
Fig. 3
figure3

Protein sizes and functional domains of photosynthetic eukaryotic KATs: a) CBP-Family Acetyltransferases, b) TAFII250-Family Acetyltransferases, c) GNAT-Family Acetyltransferases, d) MYST-Family Acetyltransferases. Each KAT family was divided by species type. These divisions include: dicot, monocot, green algae, red algae/glaucophytes, heterokont/other photosynthetic eukaryotes (cryptophytes & haptophytes) and non-photosynthetic eukaryotes. Horizontal black bars depict median protein length within a given species-type for a given KAT-family. Protein domain are depicted by colored histograms (x-axis: relative positional distribution of protein domains per depicted class of proteins, y-axis: prevalence of domain across the class of proteins)Domain information was derived from PFAM and ProSITE (Additional file 3)

Full size image

We also analyzed all KDAC and KAT ortholog protein domains using PFAM and PROSITE (Additional file 3). Each KAT family possessed at least one classifiable accessory domain, while each KDAC family consists largely of only catalytic domains (Fig. 3). Protein domain locations and composition between the different photosynthetic eukaryote species were largely conserved (e.g. no domain swapping), while key differences in KDAC and KAT domain composition between photosynthetic and non-photosynthetic eukaryotes emerged. Notably, we found differences in both green algae HDA and SRT KDACs, which have subsets of proteins (<5% of sequences analyzed) with ankyrin and peptidase auxiliary domains, respectively (Fig. 2; Additional file 3). Conversely, non-photosynthetic eukaryote HDA and SRT KDACs have an array of weakly conserved auxiliary domains (threshold >5% of proteins) including BRCT, ZF, DUF and RNASE domains (Fig. 2). HDT KDACs however, encode immense accessory domain diversity, with very few domains found in greater than 5% of the HDT proteins analyzed. This included nucleoplasmin domains in monocots and CENP-T/ZF domains in dicots.

In the photosynthetic eukaryote KATs domain differences across respective orthologs relative to non-photosynthetic eukaryotes include: (1) an N-terminal bromodomain in heterokont CBP KATs (Fig. 3a), (2) the acquisition of an ubiquitin-binding domain in monocot and dicot TAFII250 KATs (Fig. 3b), and (3) a MOZ_SAS domain exclusively in Class II (HAG2) dicot GNAT KATs (Fig. 3c). Conversely, non-photosynthetic eukaryote KATs have several highly conserved domains absent in photosynthetic eukaryotes. These include: (1) CBP N-terminal KIX and C-terminal Creb-binding domains (Fig. 3a), and (2) MYST ligase, PHD and ZF domains (Fig. 3d).

Gene expression and promoter elements of KDAC and KAT family members are conserved in Arabidopsis, poplar and rice

To extend the analysis of photosynthetic eukaryote KDAC and KAT conservation, we examined the developmental and stress-induced expression of Arabidopsis, P. trichocarpa (poplar) and O. sativa (rice) KDAC- and KAT-family orthologs in equivalent tissue types using ExpressoLog (http://bar.utoronto.ca/expressolog_treeviewer; [39]) (Additional file 2: Figure S4). ExpressoLog utilizes gene expression data from published microarray datasets to provide a comparative gene expression analysis between relative orthologs across plants [39]. Using Arabidopsis gene identifiers, the ExpressoLog tool provided us with correlative scoring (Spearman’s correlation coefficient; SCC) of class-specific Arabidopsis, poplar and rice KAT and KDAC-family ortholog gene expression during plant development and under stress. Class-specific Arabidopsis, poplar and rice KAT and KDAC-family ortholog expression during plant development was high (SCC = 0.8–1.0) except Class-I GNAT KATs (HAG1; GCN5-like; SCC = −0.6 to 0.0), suggesting a general functional conservation of KDAC and KAT protein orthologs across species (Additional file 2: Figure S4).

Next, we investigated the promoter regions of all KDAC and KAT-family genes for conserved cis-regulatory promoter elements in representative plants and algae using hypergeometric testing (Fig. 4). The identified conserved promoter elements were grouped into three categories based on functional regulation: cold/drought stress, light/circadian clock, and an additional category comprised of other or less-well characterized elements (Fig. 4; Additional file 4). Of these three groups, cold/drought stress-related elements were abundant and predominately comprised of ABRE-binding elements (Fig. 4).

Fig. 4
figure4

Enriched promoter elements in photosynthetic eukaryote KDAC and KAT gene families. Select dicots, monocots, moss and green algae (Additional file 4) were subjected to a promoter enrichment analysis as described in the Materials and Methods. Depicted are the KDAC- and KAT-families and the corresponding species- types that have significantly enriched promoter elements. Only those species-types and KDAC−/KAT-families maintaining an enriched promoter elements are depicted. Nomenclature used here describes protein family (e.g. HDA), class (e.g. I or 1) and sub-class (e.g. -3). TAFII250 represent the only exception to this nomenclature system

Full size image

Molecular phylogenetic and in silico subcellular localization analyses reveal new features of photosynthetic eukaryote KDACs and KATs

Lysine deacetylases (KDACs)

There are three families of KDACs in most photosynthetic eukaryotes. The HDA, HDT and SRT-family KDACs (Figs. 5 and 6; Additional file 2: Figure S5). HDA and SRT KDACs are found across all photosynthetic eukaryotes, while the HDT KDACs are only found in land plants (Fig. 1; Additional file 1). Consistent with their conserved role in plant development across species, the observed increase in encoded HDA KDACs parallels elevated plant complexity. Conversely, the diversity of encoded SRT KDACs decreases as plant complexity increases, with monocots and dicots lacking Class I and III SRT KDACs (Fig. 8).

Fig. 5
figure5

Consensus phylogenetic tree and subcellular localization information for Class I HDA-family KDACs from across photosynthetic and select non-photosynthetic eukaryotes. Phylogenetic tree inference and subcellular localization information was performed as outlined in the Materials and Methods. Key nodes are labelled with branch support values from 2 phylogenetic inference programs: PhyML and PhyloBayes. Node A: (1.0/0.80); Node B: (1.0/0.79); Node C: (0.95/0.75); Node D: (1.0/0.75); Node E: (0.99/0.89); Node F: (0.89/0.97); Node G: (0.89/0.97). Consensus subcellular localization information was derived from 5 prediction algorithms. Different species types and subcellular localizations are shown. Proteins without a known localization have no demarcation. Stars (*) denote proteins part of a monocot only Class 1 HDA sub-class. All sequences used in phylogenetic tree generation are listed in Additional file 3, while compiled in silico subcellular localization data can be found in Additional file 5

Full size image
Fig. 6
figure6

Consensus phylogenetic tree and subcellular localization information for Class II and IV HDA-family KDACs from across photosynthetic and select non-photosynthetic eukaryotes. Phylogenetic tree inference and subcellular localization information was performed as outlined in the Materials and Methods. Key nodes are labelled with branch support values from 2 phylogenetic inference programs: PhyML and PhyloBayes. Node A: (0.94/0.99); Node B: (0.86/0.99); Node C: (1.0/0.95); Node D: (0.98/0.96); Node E: (0.95/0.99); Node F: (0.60/0.72); Node G: (0.95/0.99); Node H: (0.93/0.71); Node I: (1.0/0.97); Node J: (0.99/0.80); Node K: (1.0/1.0); Node L: (1.0/1.0); Node M: (0.97/0.95); Node N: (0.83/0.90); Node O: (1.0/0.83); Node P: (1.0/0.97); Node Q: (0.99/1.0); Node R: (0.93/0.99); Node S: (0.89/0.82). Consensus subcellular localization information was derived from 5 prediction algorithms. Different species types and subcellular localizations are shown. Proteins without a known localization have no demarcation. Stars (*) denote a sub-class of green algae/heterokont HDA-family KDACs possessing an ankyrin domain. All sequences used in phylogenetic tree generation are listed in Additional file 3, while compiled in silico subcellular localization data can be found in Additional file 5

Full size image

HDA-family KDACs

HDA KDACs represent the most abundant KDACs encoded across photosynthetic eukaryotes. The red algae C. merolae and cryptophyte H. andersenii have the fewest HDA KDACs, while M. domestica has the most HDA KDACs (21 total). Green algae and dicots have an average of 11 HDA KDACs, while monocots average 13 (Additional file 1; Additional file 2: Figure S1). Heterokonts and representative non-photosynthetic eukaryotes have smaller numbers of HDA KDACs relative to land plants, averaging nine and five, respectively. (Additional file 1: Additional file 2: Figure S1). We found that most HDA KDACs are localized to the nucleus and cytosol, consistent with their originally described function as histone deacetylases (Figs. 5 and 6; Additional file 5); however, Class IV AtHDA2 (AtHDAj) and Class II AtHDA14 (AtHDAe) orthologs were found in different subcellular localizations between species (Fig. 6; Additional file 5). Many AtHDA2 and AtHDA14 orthologs are predicted to be localized to either the chloroplast and/or mitochondria (Fig. 6; Additional file 5).

The previously defined classes of HDA KDACs are highly conserved in all the photosynthetic eukaryotes (Figs. 5 and 6; [40]). H. sapiens (human) HDA KDACs (HsHDACs) were used in phylogenetic tree construction as a KDAC Class reference for the various classes of photosynthetic eukaryote HDA KDACs. This included HsHDAC1, 2, 3, and 8 (Class I), HsHDAC4, 5, and 7 (Class IIa) and HsHDAC6 (Class IIb) [41]. In our phylogenetic analyses, we discovered that all land plant HDA KDAC classes were derived from a green algal predecessor (Figs. 5 and 6). In land plants, each class of HDA KDACs consistently segregated by monocots and dicots, with the origins of each class anchored by the early land plants S. moellendorfii and P. patens. The higher number of monocot HDA KDACs (approximately one additional member) results from a new green algae-derived cytosolic Class I HDA KDAC family, which is exclusive to monocots (Fig. 5, node A). Interestingly, this class is absent in Z. mays (maize) and P. virgatum (Switchgrass), but is particularly expanded in rice with four members (Fig. 5 node A).

Despite family members clearly clustering as part of the Class I, II and IV, we could not identify a distinct Class IIa and b division. Furthermore, we found algae to have a number of divergent HDA KDACs basal to distinct algae/heterokont-specific HDA KDAC protein sub-classes. For example, algae and heterokonts form divergent Class II and IV HDA KDAC sub-classes that are absent in land plants (Fig. 6). Both these sub-classes were derived from either red or green algae ancestors, with the Class IV sub-class predominantly localized to the mitochondria and the Class II sub-class localized to the nucleus (Fig. 6). Overall, green algae and heterokonts maintain higher HDA KDAC diversity relative to land plants.

HDT-family deacetylases

HDT KDACs are found primarily in land plants, in which a discernible phylogenetic separation was found between monocots and dicots. Both S. moellendorfii and P. patens have HDT KDACs; however, we were not able to find HDT KDACs in glaucophytes, green, red, or brown algae (Additional file 2; Figure S5). This is consistent with other findings [42], which proposed that HDT KDACs are exclusive to land plants [36, 40, 42]. Contrastingly, our findings suggest a more ancient origin, as an HDT-family ortholog was found in the distant metazoan ancestor M. brevicolis (Fig. 7; Additional file 2: Figure S5). Similar to HDA KDACs, most HDT KDACs have a predicted nuclear and/or cytosolic localization, including the M. brevicolis ortholog (MbreHDTa) [43]. Oddly, HDT KDACs from E. huxleyi and G. theta have a predicted mitochondrial localization (Additional file 2; Figure S5, Additional file 5).

Fig. 7
figure7

Alignment of Select HDT-family KDACs from photosynthetic eukaryotes. Representative dicots (A. thaliana & P. trichocarpa), monocots (O. sativa), moss (P. patens), bryophytes (S. moellendorfii) and chromoalveolates (E. huxleyi and G. theta) are shown. The short half-life motif is conserved in the extreme n-terminus of all HDT KDACs (yellow) along with the first 100 amino acids of each HDT KDAC. Stretches of unique protein regions can be observed in M. brevicolis, G. theta and P. patens HDT KDACs (blue dashes). As well, absence of conserved land plant protein regions is also observed (shaded blue). Arrows (red) denote amino acids involved in HDT deacetylase activity. Underlined (solid red) are the larger proposed catalytic motifs. A highly conserved acidic amino acid stretch is also depicted (Underlined; solid black). M. brevecolis maintains a large n-terminal region not conserved amongst other HDT KDACs (not shown). This may be an unannotated splice variant or a mis-annotation in the M. brevicolis genome. The n-terminal methionine depicted here was highly conserved across all HDT-family KDACs found in this study

Full size image

Sirtuin (SRT)-family deacetylases

SRT KDACs are lysine deacetylases that require nicotinamide adenine dinucleotide (NAD+) as a co-factor for catalysis. This differentiates them from the metal-dependent KDACs. There are four main classes (I – IV) of SRT KDACs in eukaryotes [40, 44]. In humans these include: HsSRT1, 2 and 3 (Class I), HsSRT4 (Class II), HsSRT5 (Class III) and HsSRT6 and 7 (Class IV) [44]. Only the Class II and IV SRT KDAC orthologs that are localized to mitochondria/plastid (Class II) and nucleus/cytosol (Class IV) are found in dicots and monocots, while Class I and III orthologs are found in an array of other photosynthetic eukaryotes (Fig. 8). Relative to the non-photosynthetic eukaryotes M. brevicollis, yeast and humans, which each have an average of eight SRT KDACs, green algae and land plants encode only two or three SRTs, while moss and bryophytes encode an average of five SRT KDACs. Conversely, rhizaria, haptophytes and heterolobosea as well as one heterokont species have significantly higher numbers of SRT KDACs encoded by 13–14 genes (Additional file 1; Additional file 2; Figure S1).

Fig. 8
figure8

Consensus phylogenetic tree and subcellular localization information for SRT-family KDACs from across photosynthetic and select non-photosynthetic eukaryotes. Phylogenetic tree inference and subcellular localization information was performed as outlined in the Materials and Methods. Key nodes are labelled with branch support values from 2 phylogenetic inference programs: PhyML and PhyloBayes. Node A: (0.99/0.73); Node B: (0.99/0.97); Node C: (0.82/0.97); Node D: (0.93/0.99); Node E: (0.93/0.99); Node F: (0.94/0.99); Node G: (0.99/0.93); Node H: (0.82/0.92); Node I: (0.99/1.0); Node J: (0.79/0.75). Consensus subcellular localization information was derived from 5 prediction algorithms. Different species types and subcellular localizations are shown. Proteins without a known localization have no demarcation. All sequences used in phylogenetic tree generation are listed in Additional file 3, while compiled in silico subcellular localization data can be found in Additional file 5

Full size image

Land plant, red and green algal Class II and IV SRT KDACs consistently cluster with their human orthologs HsSRT4 (mitochondria) and HsSRT6 (cytosol/nucleus) [44], with the predicted subcellular localization of photosynthetic eukaryote Class II and IV SRT KDACs conserved (Fig. 8) [12]. Similarly, Class I HsSRTs cluster with a variety of photosynthetic eukaryote SRT KDAC orthologs independent of Class II and IV SRT KDACs (Fig. 8). The majority of these SRT KDAC orthologs have a nuclear/cytosolic subcellular localization. Basal photosynthetic eukaryote C. paradoxa encodes only a single SRT ortholog, which consistently clusters with the Class II SRT KDACs that are targeted to mitochondria/plastids, despite its predicted cytosolic localization.

Lysine acetyltransferases (KATs)

Photosynthetic eukaryotes encode 4 families of KATs: the MYST, GNAT, TAFII250 and CBP-families. Unlike the KDACs, we found that all families and classes of KATs found in non-photosynthetic eukaryotes are conserved in photosynthetic eukaryotes (Fig. 1; Additional file 1). In photosynthetic eukaryotes however, two sub-classes of CBP KATs emerged which contribute to the overall increase in photosynthetic eukaryote CBP KATs, while throughout each KAT family heterokont orthologs were found to consistently diverge from those in other photosynthetic eukaryotes (Figs. 9 and 10; Additional file 2; Figure S6 and S7).

Fig. 9
figure9

Consensus phylogenetic tree and subcellular localization information for GNAT-family KATs from across photosynthetic and select non-photosynthetic eukaryotes. Phylogenetic tree inference and subcellular localization information was performed as outlined in the Materials and Methods. Key nodes are labelled with branch support values from 2 phylogenetic inference programs: PhyML and PhyloBayes. Node A: (0.98/0.56); Node B: (0.99/0.97); Node C: (0.99/1.0); Node D: (1.0/1.0); Node E: (0.84/0.93); Node F: (0.98/0.99); Node G: (1.0/1.0); Node H: (1.0/1.0); Node I: (0.99/0.76); Node J: (0.5/0.86); Node K: (0.99/0.97); Node L: (0.94/0.97). Consensus subcellular localization information was derived from 5 prediction algorithms. Different species types and subcellular localizations are shown. Proteins without a known localization have no demarcation. All sequences used in phylogenetic tree generation are listed in Additional file 3, while compiled in silico subcellular localization data can be found in Additional file 5

Full size image
Fig. 10
figure10

Consensus phylogenetic tree and subcellular localization information for CBP-family KATs from across photosynthetic and select non-photosynthetic eukaryotes. Phylogenetic tree inference and subcellular localization information was performed as outlined in the Materials and Methods. Key nodes are labelled with branch support values from 2 phylogenetic inference programs: PhyML and PhyloBayes. Node A: (1.0/1.0); Node B: (0.87/0.91); Node C: (0.86/0.82); Node D: (1.0/1.0); Node E: (1.0/1.0); Node F: (0.95/1.0); Node G: (0.97/1.0); Node H: (0.6/0.53). Consensus subcellular localization information was derived from 5 prediction algorithms. Different species types and subcellular localizations are shown. Proteins without a known localization have no demarcation. All sequences used in phylogenetic tree generation are listed in Additional file 3, while compiled in silico subcellular localization data can be found in Additional file 5

Full size image

MYST-family acetyltransferases

MYST acetyltransferases represent a highly conserved family of protein acetylation enzymes (Additional file 2: Figure S6), with land plant MYST KATs being founded by a green algae ancestor. Green algae, heterokonts, other photosynthetic eukaryotes and land plants all encode an average of two MYST KATs, while representative non-photosynthetic eukaryotes maintained an average of four MYST KATs (Additional file 1; Additional file 2; Figure S6). The subcellular localization of MYST KATs is also conserved as most photosynthetic and non-photosynthetic orthologs have a predicted nuclear localization (Additional file 2: Figure S6). We found only one of the two green algal MYST KAT sub-classes to be basal to land plants (Additional file 2: Figure S6). As well, we found land plant MYST KATs to be encoded by closely related multi-copy families, making it likely that land plant MYSTs underwent gene duplication. This is supported by the presence of two closely related MYST KAT orthologs in P. patens. Furthermore, in Arabidopsis, MYST KATs have been found to be functionally redundant [20]; however, further examination in other organisms is required to confirm if this is an evolutionarily conserved phenomenon.

GNAT-family acetyltransferases

GNAT KATs cluster into three highly conserved protein classes in all eukaryotes. Each organism encodes a single gene copy from each of the three classes, except red algae and C. paradoxa, which have only one GNAT (Fig. 9). GNAT Class I, II and III represent the HAG1 (GCN5-like), HAG2 (HAT1-like) and HAG3 (ELP3-like) acetyltransferases; respectively. In photosynthetic eukaryotes, each class of GNAT KATs has a green algae origin. Phylogenetic analyses revealed distinct and diverse sub-classes (Class I - III) of GNAT KATs. These sub-classes are comprised of red algae and heterokont orthologs, while a diverse cluster consists of mainly heterokont proteins (Fig. 9). Class I GNAT KATs are predominantly predicted to be nuclear/cytosol localized in algae, but in land plants they are found exclusively in chloroplasts. Class III monocot orthologs are predicted to localize either to mitochondria or chloroplasts, while dicot orthologs are cytosol-localized. All Class II GNAT KATs have predicted nuclear and/or cytosol localizations.

TAFII250-family acetyltransferases

TAFII250 KATs expanded from an average of one gene in non-photosynthetic eukaryotes to two genes in monocots and dicots (Additional file 2; Figure S7). TAFII250 KATs are also found in red algae and C. paradoxa, indicating their presence in early photosynthetic eukaryotes. Many heterokonts lack a TAFII250 KAT, likely indicating gene loss in some organisms. Similar to MYST and CBP KATs, a general expansion of TAFII250 has occurred in land plants (Additional file 1; Additional file 2: Figure S7). High branch support indicates clear divisions between green algae, moss/bryophytes and higher plants, with further segregation of monocot and dicot TAFII250s (Additional file 2: Figure S7). Despite the expansion of TAFII250 KATs in some land plants, their predicted nuclear localization is highly conserved for all eukaryote TAFII250s with few exceptions (Additional file 2: Figure S7).

CBP-family acetyltransferases

CBP KATs have a complex evolutionary ancestry that has resulted in a large family expansion in land plants. They are consistently found throughout the photosynthetic eukaryotes as well as the distal non-photosynthetic eukaryote M. brevicolis (Fig. 10). Representative non-photosynthetic eukaryotes and green algae have one gene on average, while red algae and C. paradoxa encode no CBP KATs (Additional file 1; Additional file 2: Figure S1). Monocots and dicots however, encode an average of four to five CBP KATs, while moss and bryophytes have two to three. This seems to indicate ancestral gene duplication events following the colonization of land. Land plants represent the first instance of CBP segregation into Class I and II proteins (Fig. 10). Heterokonts and other photosynthetic CBP KATs reliably clustered into two classes denoted by nodes A, B and C (Fig. 10). CBP KATs have a predominantly nuclear and/or cytosol localization, although a small number of these enzymes are also predicted to localize to mitochondria or plastids.

Discussion

Reversible protein acetylation enzymes show parallels to reversible protein phosphorylation enzymes

Protein acetylation is an abundant protein post-translational modification (PTM) in all eukaryotes, second only to protein phosphorylation [7]. Similar to protein kinases (PKs) and phosphatases (PPases) that catalyze reversible protein phosphorylation, KATs and KDACs catalyze the addition and removal of acetyl groups from lysine residues (Lys-Nε) of target proteins [45]. There are several other parallels between the enzymes responsible for catalyzing reversible protein phosphorylation and acetylation that may suggest more wide-ranging evolutionary commonalties between these different regulatory PTM enzymes. For example, the four PPase families have different catalytic mechanisms ranging from diverse metal cation co-factors in PPP- (Mn2+) and PPM- (Mg2+) family PPases to cysteine and aspartate, metal-independent mechanisms in PTP and Asp-based PPases [46]. Similarly, KDACs utilize different co-factors, with HDA and SRT KDACs requiring Zn2+ and NAD+ for catalytic activity, respectively [47]. Furthermore, many PPases consist of catalytic subunits that require interaction with other proteins to achieve their specificity [48]. Accordingly, PPP-family PPases associate with hundreds of targeting subunits in mammals and other non-photosynthetic eukaryotes to determine substrate specificity [49]. Based on the compilation of KDACs (585 HDAs; 200 SRTs) from each KDAC family into representative protein models, both HDA and SRT KDACs were also consistently encoded as bare catalytic subunits in all photosynthetic eukaryotes (Fig. 2). Considering the large number of annotated proteins that are acetylated [7], it is likely that HDAs also require interactions with targeting subunits for substrate specificity. This is supported by KDAC protein interactome data from HeLa cell culture in which 200 previously uncharacterized protein complexes were found [9]. It is therefore conceivable that the HDA protein interactome in photosynthetic eukaryotes will be comparable.

Conversely, both PKs and KATs have several accessory domains that likely assist in substrate specificity. Unlike PKs however, KATs do not form a superfamily of proteins. Structural studies of non-photosynthetic eukaryote KATs indicate a diversity among the catalytic mechanisms of the MYST [50], GNAT [51] and CBP KATs [52]. Furthermore, photosynthetic and non-photosynthetic eukaryotes have fewer KATs than PKs. For example, Arabidopsis has 12 KATs compared to around 1000 PKs [53]. Considering the prevalence of protein acetylation in plants [7], this stark difference indicates that KATs likely also require different protein interaction partners to determine their substrate specificity. To date however, only a limited number of KAT protein interactome studies have been conducted in either photosynthetic or non-photosynthetic eukaryotes [54, 55]. Collectively, these commonalities suggest a form of convergent evolution amongst the enzymes responsible for catalyzing the two most prolific PTMs; phosphorylation and acetylation.

Genome scale analyses of KDAC and KAT gene families: a new understanding of origins and protein structure in photosynthetic eukaryotes

Despite photosynthetic eukaryotes possessing many of the same KDAC- and KAT-family features as their non-photosynthetic orthologs, we have identified a number of unique features, including differences in origin and protein structure. In particular, HDT KDACs, currently classified as exclusively a land plant KDAC family, were found here to originate outside of photosynthetic eukaryotes at the base of eukaryote evolution, while the CBP KATs exhibit major protein structure differences between photosynthetic and non-photosynthetic eukaryotes indicative of a conserved substitution in protein domains.

Previous reports suggested that HDT KDACs are a plant-specific KDAC family [40, 42]. Our analysis found a distant eukaryote origin of HDT KDACs in the basal non-photosynthetic eukaryote M. brevicollis (MbreHDTa), indicating that HDT KDACs are in fact not plant specific. Reciprocal BlastP analysis supports MbreHDTa as a HDT family protein, while alignment of MbreHDTa to plant HDTs reveals conservation of key HDT family motifs (Fig. 7). Further analysis of algae, heterokonts and other photosynthetic eukaryotes showed that they lack HDT KDACs, except in E. huxleyi and G. theta. This suggests either loss of HDT KDACs or an independent acquisition of HDT KDACs by photosynthetic eukaryotes. Since HDT KDACs are present in E. huxleyi and G. theta, it is most likely that HDT KDACs were lost in those photosynthetic eukaryotes that lack them.

We also found HDT KDAC protein structure to be highly divergent amongst orthologs. Only few domains are present in more than 5% of the analyzed HDT KDACs, in contrast to HDA and SRT KDACs, which are highly conserved catalytic domain-only proteins (Fig. 2). Based on the distant M. brevicollis HDT ortholog, the nucleoplasmin histone-binding domain seems to be most conserved in all organism classes and is suggested to function as a scaffold (Fig. 2) [56]. This is also reflected in the conserved domain complement of each species class, for example the nucleoplasmin domain is conserved in monocots but absent in dicots (Fig. 2; Additional file 3). Alternatively, dicot HDTs maintain a CENP-T domain. However, despite these differences, both nucleoplasmin and CENP-T domain containing proteins function to regulate chromatin [56, 57]. To date, the function of the HDT KDACs remains largely unresolved, although roles in seed germination [58] and stress response [59] have been proposed.

The CBP KAT-family has expanded in land plants (Figs. 1 and 10), beginning in moss and bryophytes with the emergence of two evolutionary distinct and conserved clusters of CBP KATs (Fig. 10). Examination of CBP KAT domain elements revealed differences in domain complements between photosynthetic and non-photosynthetic eukaryotes. Photosynthetic eukaryote CBP KATs lack the canonical kinase-inducible KIX domain (Additional file 2: Figure S8), instead maintaining a plant homeodomain (PHD) domain at a different location in the protein. Both domains allow CBP KATs to influence gene expression, but likely in different ways. The KIX domain acts as a phosphorylation-mediated docking site for transcriptional activators allowing non-photosynthetic eukaryote CBP KATs to function in protein complexes to regulate transcription [60]. The PHD domain allows photosynthetic eukaryote CBP KATs to bind methylated histones to regulate transcription in a phosphorylation independent manner [61]. Since CBP KATs remain poorly characterized in photosynthetic eukaryotes, further examination across species required to see if functional conservation exists.

Promoter element enrichment analysis provides new insights into KDAC and KAT function across species

Through comparative promoter element analysis, we found five cold/water stress response elements DRE-like, DPBF1 and 2, ABRE-like, ABFs, and CBF1BS in COR15a enriched amongst various classes and sub-classes of each KDAC and KAT family (Fig. 4). In particular, algal and monocot HDAs, monocot SRT2s as well as monocot and dicot MYSTs. Implication of involvement in stress response based on promoter elements was further supported by our ExpressoLog analysis for these protein classes and sub-classes in stress response (Additional file 2: Figure S4). For example, rice (monocot) HDA Class I-2 orthologs of AtHDAa, were found to exhibit high correlative expression across tissues under stress. Similarly, Class II SRT and MYST KDAC orthologs in rice also showed strong correlative expression under stress (Additional file 2: Figure S4). Interestingly, Class II SRT KDACs are the only known mitochondria-localized KDACs in photosynthetic eukaryotes and have been shown to regulate mitochondrial energy metabolism and metabolite transport [12]. The presence of cold and drought ABRE/ABF cis-regulatory elements in Class II SRT promoters may connect abiotic stress to adaptive responses requiring the adjustment of mitochondrial function. For example, oxidative phosphorylation complex I function has been shown to be modified by cold/drought [62] as well as ABA [63] and has also been shown to directly interact with SRT2 in Arabidopsis [12], indicating a potential connection between reversible protein acetylation and mitochondrial stress response.

In addition to enrichment of cold and drought stress response promoter elements, our analysis also found conservation of circadian- and light-responsive cis-regulatory elements in the promoters of monocot Class II SRT KDACs and Class III GNAT KATs. Considering the central nature of mitochondria to proper cell functionality, a connection between Class II SRT KDACs and light-response in plants is interesting [64]. The light-responsive promoter element HBOXCONSENSUSPVCHS may offer to connect Class II SRT KDACs to the daily fluctuations in mitochondrial metabolism [64]. Furthermore, our analysis also revealed enrichment of a CCA1-binding element [65, 66] in the promoters of Class III GNAT KATs (ELP3-KATs), which are nuclear/cytosolic proteins implicated in hormone signaling [23] and cell proliferation [67]. Both these processes are controlled by the circadian clock [68], indicating that reversible protein acetylation may also be a circadian controlled process.

Lastly, we resolved a number of ‘other’ enriched cis-regulatory promoter sequences including a nitrogen-responsive element (EMHVCHORD), a heat-stress response element (HSEs_binding_site_motif) and a flowering time-related CArG element enriched in monocot Class II-4 & -3 HDA and dicot HDT KDACs (Fig. 4). Interestingly, the Arabidopsis Class II-3 HDA KDAC ortholog ‘i’ has previously been characterized to be involved in Arabidopsis flowering, with hda-i (hda5) plants exhibiting delayed flowering and up-regulation of FLOWERING LOCUS (FLC) gene expression. This same study also showed a direct interaction between HDAi and transcription factors FVE and FLD [29]. With literature supporting many of the biological functions proposed by our cis-regulatory element enrichment analysis, further research should look to investigate KDAC and KAT Class and sub-class function in relation to roles identified as part of our cis-regulatory element enrichment analysis which have not yet been explored (e.g. a role for KDAC and KAT regulation of nitrogen responses).

Algae and heterokonts: a new frontier in understanding protein acetylation?

Algae and heterokonts represent the most diverse set of photosynthetic eukaryotes. Glaucophytes, green and red algae occupy the base of kingdom Plantae, while heterokonts emerged from algae through secondary endosymbiosis. Algae are of particular interest as the progenitors of land plants, but also because of their ability to acquire new genes via horizontal gene transfer events, leading to the acquisition and adaptation of genes with new functions and/or capabilities [69,70,71,72,73]. In light of this we examined our phylogenetic analysis for algal KDAC and KAT families. Here we found a number of unique protein sub-classes not found in land plants, but conserved amongst algae, heterokonts and other photosynthetic eukaryotes. Of these, the HDA and SRT KDACs as well as MYST and GNAT KATs have the largest number of unique protein sub-classes.

Both HDA and SRT KDACs have at least one well supported algae-containing, non-land plant protein sub-class (Figs. 5, 6 and 8). The unique SRT KDAC class is almost exclusively comprised of heterokont orthologs, which account for the major expansion of the SRT KDACs in these organisms (Fig. 8; node F). Conversely, algae and plants have a similar number of HDA KDACs as a result of likely gene duplication within one land plant Class I HDA clade (Fig. 5) combined with the increased number of unique algae/heterokont specific sub-classes. However, despite the phylogenetic diversity of these algae/heterokont KDAC sub-classes, they have minimal differences in their protein domains, suggesting that HDA and SRT KDACs are functionally conserved among the photosynthetic eukaryotes from a structure-function perspective (Fig. 2). As an exception, some phylogenetically distinct algal Class II HDA KDACs have a highly conserved Ankyrin domain in their N-terminus (Fig. 6; node H). Ankyrin domains function as protein-protein interaction platforms and are found in a variety of protein types [74], suggesting that this cluster of algae/heterokont-specific HDA KDACs may have a unique biological functions and protein interactors.

Similarly, MYST and GNAT KATs have algae/heterokont-specific protein sub-classes, respectively (Fig. 9, Additional file 2: Figure S6). Land plants and green algae both have an average of two MYST KATs; however, all land plant MYST KDACs were derived from the duplication of single green algae protein progenitor, while a second green algae-only protein sub-class founded the heterokont MYST KDACs (Additional file 2: Figure S6 node B). We also resolved a second sub-class of heterokont MYST KATs founded by red algae (Additional file 2: Figure S6 node A). The unique algae/heterokont-specific GNAT KATs are characterized by two conserved phylogenetic divisions. The first was the formation of a red algae-containing protein sub-class (Fig. 9; node I) and the second was a distinct divergence of some heterokont Class-III GNAT (HAG3; ELP3-like) KATs (Fig. 9; node H). Since respective non-photosynthetic eukaryote orthologs of N. greubi, M. brevicolis and H. sapiens appear at the base of each highly conserved GNAT KAT Class (I - III), the sub-clustering of heterokont Class-III KATs may be the result of a gene duplication event. Similar to algae/heterokont-specific MYST KATs, no differences were detected in the protein domain composition of algae/heterokont-specific GNAT KATs, indicating that they have conserved structure-function (Fig. 3). With algae and heterokonts representing a frontier of natural product discovery and biofuel production [75,76,77] identifying and characterizing proteins such as KDACs and KATs will be fundamental in better understanding how these systems are regulated.

Conclusions

Genome-scale molecular phylogenetic analyses facilitate the understanding of gene family conservation and reveal new information about protein divergence throughout evolution, such as the acquisition of new domains or re-targeting to new subcellular compartments. Our comprehensive analysis of the KDAC and KAT-families responsible for reversible protein acetylation from 53 photosynthetic eukaryotes provides an essential framework for future investigation of regulatory protein acetylation in plants. Our genome scale analysis has identified new structural elements central to the function of KDACs and KATs, including the identification of HDAs and SRTs as conserved bare catalytic subunits across photosynthetic eukaryotes. Furthermore, we resolved a number of new protein classes and sub-classes in well-established protein families; in particular a number of new algae/heterokont-specific protein sub-classes. Both algae and regulatory protein acetylation represent emerging frontiers in plant science research, rendering an understanding of reversible protein acetylation in algae and heterokonts of significant interest. For example, what are the function(s) of algal-specific KDAC/KAT gene families? Why are they not present in land plants? Future targeted studies should aim to address these open questions.

Methods

Candidate sequence isolation and validation

Protein sequences of KDAC and KAT family members were obtained from A. thaliana, P. trichocarpa (Poplar) and O. sativa (Rice) genomes using the BlastP option of Phytozome v9.1 (http://www.phytozome.org). Isolated protein sequences were employed in generating multiple sequence alignments as previously described [73]. KDAC families HDA and SRT were further divided into 2 and 3 separate alignments based on a previously annotated Class structure [40]. Within the four KAT families, only GNAT KATs were further sub-divided into three Classes, while all remaining KDAC and KAT families were aligned without further sub-division. Sequence alignments were then converted into Stockholm format and used to generate HMMs by HMMER (version 3.0) software [78]; http://hmmer.org/). A database of protein sequences from sequenced photosynthetic eukaryotes was complied with sequenced photosynthetic eukaryote genomes obtained from Phytozome (Version 9.1; http://www.phytozome.net/), Department of Energy Joint Genome Institute (DOE-JGI; http://www.jgi.doe.gov/) as well as individual genome project websites: C. merolae (http://merolae.biol.s.u-tokyo.ac.jp/); C. paradoxa (http://cyanophora.rutgers.edu/cyanophora/), E. siliculosus (http://bioinformatics.psb.ugent.be/genomes/view/Ectocarpus-siliculosus). The protein database was searched using the constructed HMMs for each protein family, with candidate sequences extracted and used in further formulation of new multiple sequence alignments as described above. HMM identified candidate orthologs from each protein family and class were filtered for a statistical threshold below e−100. All isolated HMM candidate sequences ranging in E-value from e−100 to 0.001 were manually evaluated through additional alignments and reciprocal BlastP analysis (http://blast.ncbi.nlm.nih.gov/).

Domain analysis and consensus sequence creation

To analyze putative domains from each species type (e.g. dicots) for each KDAC and KAT family, FASTA files containing protein sequences for each KDAC and KAT-family from each species type were assembled. All protein sequences used for each representative protein model were submitted to PFAM (http://pfam.xfam.org/) and PROSITE (http://prosite.expasy.org/) for domain identification analysis. The non-photosynthetic species was assembled using orthologous sequences from humans, yeast, M. brevicolis and N. gruberi. Raw outputs from each analysis can be found in Additional file 3. To summarize the information about absolute proteins size, as protein domain prevalence and domain location, we plotted for every group of proteins the median protein size as a black horizontal bar (Figs 3 and 4). For every protein, the domain information was then scaled according to the median protein size of its group. This information was then converted into colored histograms, shown on top of the black bars, indicating the frequency and location of each protein function for every group of proteins. To reduce noise, domains that were detected in less than 5% of protein sequences of a protein family within a species type were not displayed.

Gene expression and statistical analyses

Statistical comparison of each species type protein family complements was performed a non-parametric Kruskal-Wallis test in SPSS (Microsoft). Comparisons between the protein family complement of each photosynthetic eukaryote KDAC and KAT-family and the corresponding non-photosynthetic class are shown. Comparisons between each photosynthetic eukaryote species types are described in Additional file 2: Figure S1 and S2. Ortholog gene expression correlation values were obtained using Arabidopsis KDAC and KAT gene identifiers submitted to the online tool ExpressoLog ([39]; http://bar.utoronto.ca/expressolog_treeviewer/cgi-bin/expressolog_treeviewer.cgi).

Phylogenetic tree inference

Phylogenetic tree inference by both Maximum Likelihood and Bayesian methods were performed as previously described using an LG substitution model [73]. Representative tree topologies for each gene family are depicted, with support values given for each method provided at key branch points. For PhyloBayes (Bayesian method) branch support represents the posterior probability (max value = 1.00). For the maximum likelihood method (PhyML), branch support represents a Bayesian-like transformation of the approximate likelihood ratio test value (max value = 1.00). The PhyloBayes analysis was performed using the CIPRES science gateway (https://www.phylo.org/). Phylogenetic tree visualization was performed initially in FigTree (http://tree.bio.ed.ac.uk/software/figtree/), then was exported and visualized using iTOL (http://itol.embl.de/). The taxonomic tree in Fig. 1 was constructed using phyloT (http://phylot.biobyte.de/), exported using the Newick file format and edited using FigTree (http://tree.bio.ed.ac.uk/software/figtree/).

Subcellular localization prediction

Because the photosynthetic organisms we examined were diverse, we used five different in silico subcellular prediction algorithms to infer a consensus subcellular localization for each KDAC and KAT ortholog. These programs included WoLF pSORT ([79]; https://wolfpsort.hgc.jp/), TargetP ([80]; http://www.cbs.dtu.dk/services/TargetP/), SLP-Local ([81]; http://sunflower.kuicr.kyoto-u.ac.jp/~smatsuda/slplocal.html), PRedSL ([82]; http://aias.biol.uoa.gr/PredSL/input.html) and PREDOTAR ([83]; https://urgi.versailles.inra.fr/Tools/Predotar). Subsequent analysis in some cases was performed using MITOPROT ([84]; ihg.gsf.de/ihg/mitoprot.html) and ChloroP ([85]; http://www.cbs.dtu.dk/services/ChloroP/). A single subcellular location is denoted when 3/5 prediction programs indicate a single location. Alternatively, primary and secondary subcellular locations are denoted. Protein sequences without an indicated subcellular prediction lack an annotated N-terminal methionine (M). A complete output from each prediction program for each protein sequence is available in Additional file 5.

Promoter element analysis

Known promoter elements were downloaded from AtCisDB (http://arabidopsis.med.ohio-state.edu/AtcisDB/) and PLACE (http://ppdb.agr.gifu-u.ac.jp/ppdb/cgi-bin/index.cgi/) (Additional file 4). Gene location files (BioMart) and genome sequence files were downloaded from http://www.phytozome.org v11 (http://www.phytozome.org) and used to collect promoter regions of 2000 bp length, upstream of all analyzed genes. If the 5′ end was closer than 2000 bp to the end of a scaffold or chromosome, the remaining sequence was used as promoter region. Promoter regions were subsequently searched for exact, non-overlapping matches for all promoter elements (Additional file 4), tracking both number of occurrences and starting position of the individual occurrences of every element in the promoter regions of every gene. Hypergeometric testing was performed to assess enrichment of promoter elements in protein families of every species individually. Candidates genes enriched in a promoter element were selected using a 0.05 p-value cutoff (Additional file 4). Candidate promoter elements with a presence in 50% of species examined were further analyzed for conservation across species types in relation to their annotated function.

Abbreviations

CBP:

p300/CREB binding protein

GNAT:

GCN5/PCAF-related N-acetyltransferases

HDA/RPD3:

Histone deacetylase

HDT:

HD2-tuin

KAT:

Lysine acetyltransferase

KDAC:

Lysine deacetylase

MYST:

MOZ, YBF2, SAS2, and TIP60

SRT:

Sirtuin

TAFII250:

TATA binding protein-associated factors

References

  1. 1.

    Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009;325(5942):834–40.

  2. 2.

    Weinert BT, Wagner SA, Horn H, Henriksen P, Liu WR, Olsen JV, et al. Proteome-wide mapping of the drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Sci Signal. 2011;4(183):ra48.

  3. 3.

    Henriksen P, Wagner SA, Weinert BT, Sharma S, Bacinskaja G, Rehman M, et al. Proteome-wide analysis of lysine acetylation suggests its broad regulatory scope in Saccharomyces cerevisiae. Mol Cell Proteomics. 2012;11(11):1510–22.

  4. 4.

    Finkemeier I, Laxa M, Miguet L, Howden AJ, Sweetlove LJ. Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiol. 2011;155(4):1779–90.

  5. 5.

    Wu X, Oh MH, Schwarz EM, Larue CT, Sivaguru M, Imai BS, et al. Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol. 2011;155(4):1769–78.

  6. 6.

    Lundby A, Lage K, Weinert BT, Bekker-Jensen DB, Secher A, Skovgaard T, et al. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep. 2012;2(2):419–31.

  7. 7.

    Rao RS, Thelen JJ, Miernyk JA. Is Lys-Nvarepsilon-acetylation the next big thing in post-translational modifications? Trends Plant Sci. 2014;19(9):550–3.

  8. 8.

    Alinsug MV, Chen FF, Luo M, Tai R, Jiang L, Wu K. Subcellular localization of class II HDAs in Arabidopsis thaliana: nucleocytoplasmic shuttling of HDA15 is driven by light. PLoS One. 2012;7(2):e30846.

  9. 9.

    Joshi P, Greco TM, Guise AJ, Luo Y, Yu F, Nesvizhskii AI, et al. The functional interactome landscape of the human histone deacetylase family. Molecular Syst Biol. 2013;9:672.

  10. 10.

    Liu X, Luo M, Zhang W, Zhao J, Zhang J, Wu K, et al. Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol. 2012;12:145.

  11. 11.

    Tran HT, Nimick M, Uhrig RG, Templeton G, Morrice N, Gourlay R, et al. Arabidopsis thaliana Histone deacetylase 14 (HDA14) is an alpha-tubulin deacetylase that associates with PP2A and enriches in the microtubule fraction with the putative histone acetyltransferase ELP3. Plant J. 2012;71(2):263–72.

  12. 12.

    Konig AC, Hartl M, Pham PA, Laxa M, Boersema PJ, Orwat A, et al. The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiol. 2014;164(3):1401–14.

  13. 13.

    Nallamilli BR, Edelmann MJ, Zhong X, Tan F, Mujahid H, Zhang J, et al. Global analysis of lysine acetylation suggests the involvement of protein acetylation in diverse biological processes in rice (Oryza sativa). PLoS One. 2014;9(2):e89283.

  14. 14.

    Xiong Y, Peng X, Cheng Z, Liu W, Wang GL. A comprehensive catalog of the lysine-acetylation targets in rice (Oryza sativa) based on proteomic analyses. J Proteomic. 2016;138:20–9.

  15. 15.

    Smith-Hammond CL, Swatek KN, Johnston ML, Thelen JJ, Miernyk JA. Initial description of the developing soybean seed protein Lys-N-epsilon -acetylome. J Proteomic. 2014;96:56–66.

  16. 16.

    Melo-Braga MN, Verano-Braga T, Leon IR, Antonacci D, Nogueira FC, Thelen JJ, et al. Modulation of protein phosphorylation, N-glycosylation and Lys-acetylation in grape (Vitis vinifera) mesocarp and exocarp owing to Lobesia botrana infection. Mol Cell Proteomics. 2012;11(10):945–56.

  17. 17.

    Smith-Hammond CL, Hoyos E, Miernyk JA. The pea seedling mitochondrial N-epsilon-lysine acetylome. Mitochondrion. 2014;19:154–65.

  18. 18.

    Zhang Y, Song L, Liang W, Mu P, Wang S, Lin Q. Comprehensive profiling of lysine acetylproteome analysis reveals diverse functions of lysine acetylation in common wheat. Sci Rep. 2016;6:21069.

  19. 19.

    Papaefthimiou D, Likotrafiti E, Kapazoglou A, Bladenopoulos K, Tsaftaris A. Epigenetic chromatin modifiers in barley: III. Isolation and characterization of the barley GNAT-MYST family of histone acetyltransferases and responses to exogenous ABA. Plant Physiol Biochem. 2010;48(2–3):98–107.

  20. 20.

    Latrasse D, Benhamed M, Henry Y, Domenichini S, Kim W, Zhou DX, et al. The MYST histone acetyltransferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol. 2008;8:121.

  21. 21.

    Xiao J, Zhang H, Xing L, Xu S, Liu H, Chong K, et al. Requirement of histone acetyltransferases HAM1 and HAM2 for epigenetic modification of FLC in regulating flowering in Arabidopsis. J Plant Physiol. 2013;170(4):444–51.

  22. 22.

    Defraia CT, Wang Y, Yao J, Mou Z. Elongator subunit 3 positively regulates plant immunity through its histone acetyltransferase and radical S-adenosylmethionine domains. BMC Plant Biol. 2013;13:102.

  23. 23.

    Nelissen H, De Groeve S, Fleury D, Neyt P, Bruno L, Bitonti MB, et al. Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. Proc Natl Acad Sci U S A. 2010;107(4):1678–83.

  24. 24.

    Benhamed M, Bertrand C, Servet C, Zhou DX. Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell. 2006;18(11):2893–903.

  25. 25.

    Han SK, Song JD, Noh YS, Noh B. Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 2007;49(1):103–14.

  26. 26.

    Heisel TJ, Li CY, Grey KM, Gibson SI. Mutations in HISTONE ACETYLTRANSFERASE1 affect sugar response and gene expression in Arabidopsis. Front Plant Sci. 2013;4:245.

  27. 27.

    Li C, Xu J, Li J, Li Q, Yang H. Involvement of Arabidopsis histone acetyltransferase HAC family genes in the ethylene signaling pathway. Plant Cell Physiol. 2014;55(2):426–35.

  28. 28.

    Lindner M, Simonini S, Kooiker M, Gagliardini V, Somssich M, Hohenstatt M, et al. TAF13 interacts with PRC2 members and is essential for Arabidopsis seed development. Dev Biol. 2013;379(1):28–37.

  29. 29.

    Luo M, Tai R, Yu CW, Yang S, Chen CY, Lin WD, et al. Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J. 2015;82(6):925–36.

  30. 30.

    Cigliano RA, Cremona G, Paparo R, Termolino P, Perrella G, Gutzat R, et al. Histone deacetylase AtHDA7 is required for female gametophyte and embryo development in Arabidopsis. Plant Physiol. 2013;163(1):431–40.

  31. 31.

    Liu X, Chen CY, Wang KC, Luo M, Tai R, Yuan L, et al. PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell. 2013;25(4):1258–73.

  32. 32.

    Gu X, Jiang D, Yang W, Jacob Y, Michaels SD, He Y. Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLoS Genet. 2011;7(11):e1002366.

  33. 33.

    Liu C, Li LC, Chen WQ, Chen X, Xu ZH, Bai SN. HDA18 affects cell fate in Arabidopsis root epidermis via histone acetylation at four kinase genes. Plant Cell. 2013;25(1):257–69.

  34. 34.

    Wang Z, Cao H, Sun Y, Li X, Chen F, Carles A, et al. Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell. 2013;25(1):149–66.

  35. 35.

    Choi SM, Song HR, Han SK, Han M, Kim CY, Park J, et al. HDA19 is required for the repression of salicylic acid biosynthesis and salicylic acid-mediated defense responses in Arabidopsis. Plant J. 2012;71(1):135–46.

  36. 36.

    Grandperret V, Nicolas-Frances V, Wendehenne D, Bourque S. Type-II histone deacetylases: elusive plant nuclear signal transducers. Plant Cell Environ. 2014;37(6):1259–69.

  37. 37.

    Shurin JB, Burkart MD, Mayfield SP, Smith VH. Recent progress and future challenges in algal biofuel production. F1000Res. 2016;4(5). doi:10.12688/f1000research.9217.1.

  38. 38.

    Bhullar NK, Gruissem W. Nutritional enhancement of rice for human health: the contribution of biotechnology. Biotechnol Adv. 2013;31(1):50–7.

  39. 39.

    Patel RV, Nahal HK, Breit R, Provart NJ. BAR expressolog identification: expression profile similarity ranking of homologous genes in plant species. Plant J. 2012;71(6):1038–50.

  40. 40.

    Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, et al. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 2002;30(23):5036–55.

  41. 41.

    Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res. 2007;5(10):981–9.

  42. 42.

    Bourque S, Jeandroz S, Grandperret V, Lehotai N, Aime S, Soltis DE, et al. The evolution of HD2 proteins in green plants. Trends Plant Sci. 2016;21(12):1008–16.

  43. 43.

    Luo M, Wang YY, Liu X, Yang S, Wu K. HD2 proteins interact with RPD3-type histone deacetylases. Plant Signal Behav. 2012;7(6):608–10.

  44. 44.

    Frye RA. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun. 2000;273(2):793–8.

  45. 45.

    Choudhary C, Weinert BT, Nishida Y, Verdin E, Mann M. The growing landscape of lysine acetylation links metabolism and cell signalling. Nat Rev. Mol Cell Biol. 2014;15(8):536–50.

  46. 46.

    Uhrig RG, Labandera AM, Moorhead GB. Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci. 2013;18(9):505–13.

  47. 47.

    Wang XW, Guo LY, Han M, Shan K. Diversity, evolution and expression profiles of histone acetyltransferases and deacetylases in oomycetes. BMC Genomics. 2016;17(1):927.

  48. 48.

    Moorhead GB, De Wever V, Templeton G, Kerk D. Evolution of protein phosphatases in plants and animals. Biochem J. 2009;417(2):401–9.

  49. 49.

    Heroes E, Lesage B, Gornemann J, Beullens M, Van Meervelt L, Bollen M. The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J. 2013;280(2):584–95.

  50. 50.

    Berndsen CE, Albaugh BN, Tan S, Denu JM. Catalytic mechanism of a MYST family histone acetyltransferase. Biochemistry. 2007;46(3):623–9.

  51. 51.

    Tanner KG, Trievel RC, Kuo MH, Howard RM, Berger SL, Allis CD, et al. Catalytic mechanism and function of invariant glutamic acid 173 from the histone acetyltransferase GCN5 transcriptional coactivator. J Biol Chem. 1999;274(26):18157–60.

  52. 52.

    Liu X, Wang L, Zhao K, Thompson PR, Hwang Y, Marmorstein R, et al. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature. 2008;451(7180):846–50.

  53. 53.

    Zulawski M, Schulze G, Braginets R, Hartmann S, Schulze WX. The Arabidopsis Kinome: phylogeny and evolutionary insights into functional diversification. BMC Genomics. 2014;15:548.

  54. 54.

    Smart SK, Mackintosh SG, Edmondson RD, Taverna SD, Tackett AJ. Mapping the local protein interactome of the NuA3 histone acetyltransferase. Protein Sci. 2009;18(9):1987–97.

  55. 55.

    Mitchell L, Huard S, Cotrut M, Pourhanifeh-Lemeri R, Steunou AL, Hamza A, et al. mChIP-KAT-MS, a method to map protein interactions and acetylation sites for lysine acetyltransferases. Proc Natl Acad Sci U S A. 2013;110(17):E1641–50.

  56. 56.

    Frehlick LJ, Eirin-Lopez JM, Ausio J. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. BioEssays. 2007;29(1):49–59.

  57. 57.

    Nishino T, Takeuchi K, Gascoigne KE, Suzuki A, Hori T, Oyama T, et al. CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell. 2012;148(3):487–501.

  58. 58.

    Colville A, Alhattab R, Hu M, Labbe H, Xing T, Miki B. Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep. 2011;30(10):1969–79.

  59. 59.

    Han Z, Yu H, Zhao Z, Hunter D, Luo X, Duan J, et al. AtHD2D Gene plays a role in plant growth, development, and response to Abiotic stresses in Arabidopsis thaliana. Frontiers Plant Sci. 2016;7:310.

  60. 60.

    Novatchkova M, Eisenhaber F. Linking transcriptional mediators via the GACKIX domain super family. Curr Biol. 2004;14(2):R54–5.

  61. 61.

    Fortschegger K, Shiekhattar R. Plant homeodomain fingers form a helping hand for transcription. Epigenetics. 2011;6(1):4–8.

  62. 62.

    Lee BH, Lee H, Xiong L, Zhu JK. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell. 2002;14(6):1235–51.

  63. 63.

    He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, et al. DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell. 2012;24(5):1815–33.

  64. 64.

    Lee CP, Eubel H, Millar AH. Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis. Mol Cell Proteomics. 2010;9(10):2125–39.

  65. 65.

    Andronis C, Barak S, Knowles SM, Sugano S, Tobin EM. The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol Plant. 2008;1(1):58–67.

  66. 66.

    Michael TP, McClung CR. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol. 2003;132(2):629–39.

  67. 67.

    Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, Traas J, et al. The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc Natl Acad Sci U S A. 2005;102(21):7754–9.

  68. 68.

    Greenham K, McClung CR. Integrating circadian dynamics with physiological processes in plants. Nat Rev. Genet. 2015;16(10):598–610.

  69. 69.

    Keeling PJ. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev. 2009;19(6):613–9.

  70. 70.

    Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev. Genet. 2008;9(8):605–18.

  71. 71.

    Raymond JA, Kim HJ. Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS One. 2012;7(5):e35968.

  72. 72.

    Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A. 2006;103(31):11647–52.

  73. 73.

    Uhrig RG, Kerk D, Moorhead GB. Evolution of bacterial-like phosphoprotein phosphatases in photosynthetic eukaryotes features ancestral mitochondrial or archaeal origin and possible lateral gene transfer. Plant Physiol. 2013;163(4):1829–43.

  74. 74.

    Bork P. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins. 1993;17(4):363–74.

  75. 75.

    Blunt JW, Copp BR, Keyzers RA, Munro MH, Prinsep MR. Marine natural products. Nat Prod Rep. 2015;32(2):116–211.

  76. 76.

    Fernando IP, Nah JW, Jeon YJ. Potential anti-inflammatory natural products from marine algae. Environ Toxicol Pharmacol. 2016;48:22–30.

  77. 77.

    Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, et al. Microalgae biorefinery: high value products perspectives. Bioresour Technol. 2017;229:53–62.

  78. 78.

    Eddy SR. Profile hidden Markov models. Bioinformatics. 1998;14(9):755–63.

  79. 79.

    Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35(Web Server issue):W585–7.

  80. 80.

    Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000;300(4):1005–16.

  81. 81.

    Matsuda S, Vert JP, Saigo H, Ueda N, Toh H, Akutsu T. A novel representation of protein sequences for prediction of subcellular location using support vector machines. Protein Sci. 2005;14(11):2804–13.

  82. 82.

    Petsalaki EI, Bagos PG, Litou ZI, Hamodrakas SJ. PredSL: a tool for the N-terminal sequence-based prediction of protein subcellular localization. Genomics Proteomics Bioinformatics. 2006;4(1):48–55.

  83. 83.

    Small I, Peeters N, Legeai F, Lurin C. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics. 2004;4(6):1581–90.

  84. 84.

    Claros MG, Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem. 1996;241(3):779–86.

  85. 85.

    Emanuelsson O, Nielsen H, von Heijne G. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 1999;8(5):978–84.

Download references

Acknowledgments

The authors would like to thank Dr. David Kerk (University of Calgary) and Dr. Johannes Fütterer (ETH Zurich) for helpful discussions and Dr. Timothy Paape (University of Zurich) for critical reading of the manuscript.

Funding

This work was made possible by funding from ETH Zurich, the European Union Seventh Framework Programme for research, technological development and demonstration under grant agreement no GA-2010-267,243 – PLANT FELLOWS and GA–2013–608,422–IDP BRIDGES, as well as the Natural Sciences and Engineering Research Council (NSERC) of Canada. None of the aforementioned agencies directly participated in study design, data collection, analysis, and interpretation nor manuscript writing.

Availability of data and materials

The data supporting the conclusions of this article are included in its additional files and the publically available repositories from which it was derived. This includes: Phytozome (http://www.phytozome.net/) and Department of Energy Joint Genome Institute (DOE-JGI; http://www.jgi.doe.gov/) as well as Additional file 3 for protein sequence information. PFAM (http://pfam.xfam.org/), PROSITE (http://prosite.expasy.org/), and Additional file 3 for all protein structure data. Additional file 5 for all subcellular localization information. AtCisDB (http://arabidopsis.med.ohio-state.edu/AtcisDB/), PLACE (https://sogo.dna.affrc.go.jp/) and Additional file 4 for all promoter element data. Lastly, data involving gene expression comparison between species can be found at http://bar.utoronto.ca/expressolog_treeviewer/cgi-bin/expressolog_treeviewer.cgi. No database permissions were required for accessing the data used in this study except for the Department of Energy Joint Genomic Institute which now requires users register for a free account to download data.

Author information

Affiliations

  1. Department of Biology, Institute of Molecular Plant Biology, ETH Zurich, Universitätstrasse 2, 8092, Zurich, Switzerland

    • R. Glen Uhrig
    • , Pascal Schläpfer
    • , Devang Mehta
    • , Matthias Hirsch-Hoffmann
    •  & Wilhelm Gruissem

  2. Plant Biology Department, Carnegie Institution for Science, Stanford, CA, 94305, USA

    • Pascal Schläpfer

Authors

  1. Search for R. Glen Uhrig in:

  2. Search for Pascal Schläpfer in:

  3. Search for Devang Mehta in:

  4. Search for Matthias Hirsch-Hoffmann in:

  5. Search for Wilhelm Gruissem in:

Contributions

RGU conceived the study, performed HMM, subcellular localization and phylogenetic tree analyses. PS performed promoter enrichment and protein domain analyses. DM performed data analysis involving promoter elements and taxonomy. MHH assisted in identifying and annotating promoter sequences. RGU, PS, DM and WG contributed to data discussions, manuscript writing and assembly. All authors have read and approved the manuscript for publication.

Corresponding author

Correspondence to R. Glen Uhrig.

Ethics declarations

Ethics approval and consent to participate

No plants or other organisms were used in this study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Additional files

Additional file 1:

Tabulation of KDAC and KAT-family members from across photosynthetic eukaryotes. (XLSX 18 kb)

Additional file 2:

Supplemental Figures S1–S8. (PDF 25600 kb)

Additional file 3:

All protein sequences used as well as PFAM and ProSITE domain analysis raw output. (XLSX 10502 kb)

Additional file 4:

All promoter element analysis data: raw, processed and summary. (XLSX 6425 kb)

Additional file 5:

All in silico subcellular localization prediction raw data. (XLSX 516 kb)

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Keywords

  • Protein Acetylation
  • Photosynthetic eukaryotes
  • Post-translational modifications
  • Lysine Acetyltransferase
  • Lysine Deacetylase
  • Genomics

BMC Genomics

ISSN: 1471-2164

Contact us