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

Abstract

BackgroundReversible 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3894-0) contains supplementary material, which is available to authorized users.

Diurnal changes in concerted plant protein phosphorylation and acetylation in Arabidopsis organs and seedlings

“…Much less is known about the substrate preferences of protein acetyltransferases because protein acetylation occurring outside of nuclear chromatin regulation has only been investigated more recently (Choudhary et al ., ; Weinert et al ., ; Henriksen et al ., ). Given the large number of acetylation events and the low number of protein acetyltransferases, it is likely that acetyltransferases function as part of multiprotein complexes to determine their substrate specificity (Uhrig et al ., ). In accordance with our analysis of protein phosphorylation motifs and their corresponding substrate networks, we similarly examined acetylation motifs and their substrate networks.…”

“…In particular, plastid proteins with AcKY and [I/L]AcK motifs form large association networks covering a wide range of chloroplast processes (Figure S6; Data S20). With only a few KATs (AtGNATa/AtCBPc) and KDACs (AtHDA14) either predicted (Uhrig et al ., ) or verified (Hartl et al ., ) to be localized to the chloroplast, it is likely that each forms multiple protein complexes to target the diversity of proteins with these motifs. Currently there is little known about these motifs, and there have been few specific studies connecting these protein acetylation motifs with the activities of specific acetyltransferases or deacetylases.…”

“…The diurnal fluctuations in the abundance that we find for both protein phosphorylation and acetylation events on light-harvesting and photosystems proteins suggest that these proteins represent key intersecting nodes of signaling and metabolism. Only a single lysine deacetylase (AtHDA14, At4g33470) and three acetyltransferases (AtGNATa, At3g54610; AtCBPc, At1g55970; and NSI1, At1g32070) have been identified as plastidial (Hartl et al, 2017;Uhrig et al, 2017;Koskela et al, 2018), suggesting that substrate specificity for these enzymes must be achieved through the formation of specific but currently unknown protein complexes similar to phosphoprotein phosphatase (PPP)-family phosphatases .…”

“…Less is known about protein acetylation in plants (Rao et al, 2014), although recent studies in Arabidopsis (Finkemeier et al, 2011;Wu et al, 2011;Hartl et al, 2017), Oryza sativa (rice) (Nallamilli et al, 2014), Pisum sativum (pea) (Smith-Hammond et al, 2014a), Glycine max (soybean) (Smith-Hammond et al, 2014b) and Triticum aestivum (wheat) (Zhang et al, 2016) have provided first insights into the extent of plant protein acetylation. Similar to kinases and phosphatases involved in protein phosphorylation, protein acetylation is catalyzed by two families: the lysine acetyltransferases (KATs) and the lysine deacetylases (KDACs), which catalyze the addition and removal of acetyl groups from target proteins, respectively (Pandey et al, 2002;Tran et al, 2012b;Uhrig et al, 2017). Both protein phosphorylation and acetylation have been shown to regulate key cellular processes, such as glycolysis, nitrogen metabolism, photosynthesis (Finkemeier et al, 2011;Engelsberger and Schulze, 2012;Menz et al, 2016) and development (Han et al, 2016;Zhao et al, 2017).…”

A Journey Through Plant Cytoskeleton: Hot Spots in Signaling and Functioning

“…Reversible protein acetylation occurring on Lys‐N e has emerged as a key regulatory post‐translational modification in eukaryotes (Uhrig et al, ), including plant tubulin (Smertenko et al, ). Besause MTs are highly conserved protein structures, the interaction of MT elements with MT‐associated proteins and post‐translational modifiers is fully dependent on protein interfaces, and almost all MT modifications are well described except acetylation.…”