The Evolution of HD2 Proteins in Green Plants

Bourque, Stéphane; Jeandroz, Sylvain; Grandperret, Vincent; Lehotai, Nóra; Aimé, Sébastien; Soltis, Douglas E.; Miles, Nicholas W.; Melkonian, Michael; Deyholos, Michael K.; Leebens‐Mack, Jim; Chase, Mark W.; Rothfels, Carl J.; Stevenson, Dennis Wm.; Graham, Sean W.; Wang, X.; Wu, Shuangxiu; Pires, J. Chris; Edger, Patrick P.; Yan, Zhixiang; Xie, Yeming; Carpenter, Eric J.; Wong, Gane Ka‐Shu; Wendehenne, David; Nicolas-Francès, Valérie

doi:10.1016/j.tplants.2016.10.001

Cited by 41 publications

(64 citation statements)

References 24 publications

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“…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.…”

Section: Resultssupporting

confidence: 93%

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

et al. 2017

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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.

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Section: Resultssupporting

confidence: 93%

“…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.…”

Section: Discussionmentioning

confidence: 41%

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

et al. 2017

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“…The HD2 proteins share a conserved N-terminal nucleoplasminlike (NPL) domain (Supplemental Figure 3B) predicted to be a catalytic domain (Bourque et al, 2016). The conserved first five residues (MEFWG), the histidine at position 25 (H25), and the aspartic/glutamic acid at position 69 (D/E69) are critical to the deacetylation activity (indicated with square and asterisks in Supplemental Figure 3B) (Zhou et al, 2004).…”

Section: Hd2c Interacts With Hd2b and Forms A Homo-oligomermentioning

confidence: 99%

“…In the flowering plant Arabidopsis thaliana, RPD3-like histone deacetylase HDA6 is required for the suppression of silenced rDNA loci (Probst et al, 2004;Earley et al, 2006Earley et al, , 2010Pontes et al, 2007;Pontvianne et al, 2013). Besides the conserved RPD3 and SIR proteins, Arabidopsis has an additional plant-specific HDAC family, termed type-2 HDACs (HD2s), that are phylogenetically conserved in green plants (Bourque et al, 2016). HD2A represses rDNA transcription in nucleolar dominance (Pontes et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Canonical and Noncanonical Actions of Arabidopsis Histone Deacetylases in Ribosomal RNA Processing

et al. 2018

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Ribosome biogenesis is a fundamental process required for all cellular activities. Histone deacetylases play critical roles in many biological processes including transcriptional repression and rDNA silencing. However, their function in pre-rRNA processing remains poorly understood. Here, we discovered a previously uncharacterized role of histone deacetylase HD2C in pre-rRNA processing via both canonical and noncanonical manners. HD2C interacts with another histone deacetylase HD2B and forms homo- and/or hetero-oligomers in the nucleolus. Depletion of HD2C and HD2B induces a ribosome-biogenesis deficient phenotype and aberrant accumulation of 18S pre-rRNA intermediates. Our genome-wide analysis revealed that HD2C binds and represses the expression of key genes involved in ribosome biogenesis. Using RNA immunoprecipitation and sequencing, we further uncovered a noncanonical mechanism of HD2C directly associating with pre-rRNA and small nucleolar RNAs to regulate rRNA methylation. Together, this study reveals a multifaceted role of HD2C in ribosome biogenesis and provides mechanistic insights into how histone deacetylases modulate rRNA maturation at the transcriptional and posttranscriptional levels.

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“…Phylogenetic analysis has classified HDACs into three distinct families, namely RPD3/HDA1-like HDACs, SIR2-like HDACs, and HD2 proteins, based on sequence similarity, substrate specificity, and cofactor requirement Bourque et al, 2016). The majority of the HDACs in a given plant species are of the RPD3/HDA1-like category; for example, Arabidopsis thaliana has 12 RPD3/HDA1 subfamily genes among 18 putative HDAC family genes .…”

Section: Introductionmentioning

confidence: 99%

Overexpression of <em>AhHDA1</em> Results in Retarded Growth of Hairy Roots and Altered Cell Metabolism in <em>Arachis hypogaea</em>

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S²,

Liu³

et al. 2018

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Peanut (Arachis hypogaea) is a crop plant with high economic value, but the epigenetic regulation of its growth and development has only rarely been studied. The peanut histone deacetylase 1 gene (AhHDA1) has been isolated and is known to be ABA-and drought-responsive. In this paper, we investigate the role of AhHDA1 in more detail, focussing on the effect of altered AhHDA1 expression in hairy roots at both the phenotypic and transcriptional levels. Agrobacterium rhizogenes-mediated transformation of A. hypogaea hairy roots was used to analyse how overexpression or RNA interference of AhHDA1 affects this tissue. In both types of transgenic hairy root, RNA sequencing was adopted to identify genes that were differentially expressed, and these genes were assigned to specific metabolic pathways. AhHDA1-overexpressing hairy roots were growth-retarded after 20 d in vitro cultivation, and superoxide anions and hydrogen peroxide accumulated to a greater extent than in control or RNAi groups. Overexpression of AhHDA1 is likely to accelerate flux through various secondary synthetic metabolic pathways in hairy roots, as well as reduce photosynthesis and oxidative phosphorylation. Genes encoding the critical enzymes caffeoyl-CoA O-methyltransferase (Araip.XGB85) and caffeic acid 3-O-methyltransferase (Araip.Z3XZX) in the phenylpropanoid biosynthesis pathway, chalcone synthase (Araip.B8TJ0) and polyketide reductase (Araip.MKZ27) in the flavonoid biosynthesis pathway, and hydroxyisoflavanone synthase (Araip.0P3RJ) and isoflavone 2'-hydroxylase (Araip.S5EJ7) in the isoflavonoid biosynthesis pathway were significantly upregulated by AhHDA1 overexpression, while their expression in AhHDA1-RNAi and control hairy roots remained at a lower level or was unchanged. Our results suggest that alteration of secondary Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 25 3 metabolism activities is related to overexpression of AhHDA1, which is mainly reflected in phenylpropanoid, flavonoid and flavonoid biosynthesis. Future studies will focus on the function of AhHDA1 interacting proteins and their action on cell growth and stress responses.

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The Evolution of HD2 Proteins in Green Plants

Cited by 41 publications

References 24 publications

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

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

Canonical and Noncanonical Actions of Arabidopsis Histone Deacetylases in Ribosomal RNA Processing

Overexpression of <em>AhHDA1</em> Results in Retarded Growth of Hairy Roots and Altered Cell Metabolism in <em>Arachis hypogaea</em>

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