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Communication Comprehensive Analysis of the Histone Deacetylase Gene Family in Chinese Cabbage (Brassica rapa): From Evolution and Expression Pattern to Functional Analysis of BraHDA3 Seung Hee Eom and Tae Kyung Hyun * Department of Industrial Plant Science and Technology, Chungbuk National University, Cheongju 28644, Korea; eom0214@naver.com * Correspondence: taekyung7708@chungbuk.ac.kr; Tel. +82‐43‐261‐2520 Abstract: Histone deacetylases (HDACs) are known as erasers that remove acetyl groups from ly‐ sine residues in histones. Although plant HDACs play essential roles in physiological processes, including various stress responses, our knowledge concerning HDAC gene families and their evo‐ lutionary relationship remains limited. In Brassica rapa genome, we identified 20 HDAC genes, which are divided into three major groups: RPD3/HDA1, HD2, and SIR2 families. In addition, seven pairs of segmental duplicated paralogs and one pair of tandem duplicated paralogs were identified in the B. rapa HDAC (BraHDAC) family, indicating that segmental duplication is predominant for the expansion of the BraHDAC genes. The expression patterns of paralogous gene pairs suggest a divergence in the function of BraHDACs under various stress conditions. Furthermore, we sug‐ Citation: Eom, S.H.; Hyun, T.K. gested that BraHDA3 (homologous of Arabidopsis HDA14) encodes the functional HDAC enzyme, Comprehensive Analysis of the which can be inhibited by Class I/II HDAC inhibitor SAHA. As a first step toward understanding Histone Deacetylase Gene Family in the epigenetic responses to environmental stresses in Chinese cabbage, our results provide a solid Chinese cabbage (Brassica rapa): foundation for functional analysis of the BraHDAC family. From Evolution and Expression Pattern to Functional Analysis of Keywords: Chinese cabbage; duplication; epigenetics; histone deacetylase BraHDA3. Agriculture 2021, 11, 244. https://doi.org/10.3390/ agriculture11030244 1. Introduction Academic Editor: Kevin Begcy Epigenetic regulation, including DNA and histone modifications, plays an essential and Laramy Enders role in controlling chromatin structure, with the nucleosome as the basic organization unit Received: 24 February 2021 [1]. In eukaryotes, post‐transcriptional histone modifications such as acetylation, methyl‐ Accepted: 10 March 2021 ation, ubiquitination, and sumoylation enable the regulation of mRNA expression by re‐ Published: 12 March 2021 cruiting histone writers, erasers, and readers [2]. Among these modifications, histone acet‐ ylation in different lysine residues of histones by histone acetyltransferases (HATs) is re‐ Publisher’s Note: MDPI stays neu‐ quired for opening the chromatin structure to allow binding of RNA polymerase II and tral with regard to jurisdictional transcription factors; in contrast, histone deacetylases (HDACs) maintain the homeotic claims in published maps and insti‐ balance of histone acetylation by removing the acetyl groups from hyperacetylated his‐ tutional affiliations. tones [1,3]. The highly dynamic balance of the histone acetylation and deacetylation is mostly maintained by the physical and functional interplay between HAT and HDAC activities [3], and serves as a major epigenetic regulatory mechanism for gene transcrip‐ tion and in turn governs numerous physiological processes [4]. Copyright: © 2021 by the authors. In higher plants, HDACs are generally classified into three distinct groups: the re‐ Licensee MDPI, Basel, Switzerland. duced potassium dependence 3/histone deacetylase 1 (RPD3/HDA1) family, silent infor‐ This article is an open access article mation regulator 2 (SIR2) family, and histone deacetylase 2 (HD2) family [5]. Since 18 distributed under the terms and HDACs were identified in the Arabidopsis thaliana genome [6], several HDACs have been conditions of the Creative Commons Attribution (CC BY) license identified and isolated from rice [7], soybean [8], grape [9], litchi [10], maize [11], and (http://creativecommons.org/licenses cotton [12]. These indicate that genome‐wide mining and comparative analysis are pow‐ /by/4.0/). erful approach to identify genes and understand the evolutionary relationships of genes. Agriculture 2021, 11, 244. https://doi.org/10.3390/agriculture11030244 www.mdpi.com/journal/agriculture Agriculture 2021, 11, 244 2 of 10 Genetic and physiological studies on Arabidopsis have shown that HDA6, HDA9, HDA15, HDA19, HD2C, and AtSRT1 negatively regulate stress tolerance by regulating gene ex‐ pression through histone acetylation [13]. The Arabidopsis HDA6 mutants showed en‐ hanced induction of genes involved in the acetate biosynthesis pathway, which resulted in enhanced drought tolerance [14]. Similarly, the loss‐of‐function of HDA9 showed in‐ creased tolerance against salt and drought stresses [15]. In addition, HDA19‐deficiency enhanced tolerance to high‐salinity, drought, and heat stresses in Arabidopsis [16]. In con‐ trast, HDA19 overexpression in Arabidopsis enhanced disease resistance against Alternaria brassicicola via increased transcription of jasmonic acid and ethylene responsive genes [17]. In rice plants, overexpression of OsHDA705, a member of the RPD3/HDA1 family, re‐ sulted in decreased salt and abscisic acid (ABA) stress tolerance during seed germination, whereas its overexpression resulted in enhanced osmotic stress resistance during the seed‐ ling stage [18]. The decrease in levels of histone H4 acetylation because of the overexpres‐ sion of OsHDT701 (rice HD2 family) caused reduced resistance against rice pathogens Magnaporthe oryzae and Xanthomonas oryzae pv oryzae [7], whereas the overexpression of HDT701 in transgenic rice leads to increased tolerance to NaCl and polyethylene glycol stresses [19]. Furthermore, mitogen‐activated protein kinase 3 phosphorylates the histone deacetylase HD2B to control the transcription of biotic stress response genes [20]. Collec‐ tively, these indicate the importance, diversity, and specificity of HDACs in response to different stimuli. Despite the knowledge concerning HDACs, the evolutionary relationships and func‐ tional information regarding the HDAC family in Brassica rapa, a crop species of economic importance, remain largely unknown. In this study, we aimed at genome‐wide identifica‐ tion of the HDAC gene family in B. rapa genome. Expansion and evolutionary mechanisms of this gene family were studied to explore the evolutionary relationships among B. rapa HDAC family (BraHDAC). Furthermore, we analyzed the expression pattern of BraHDACs under different abiotic stress condition, providing valuable information for further study of BraHDAC gene functions. 2. Materials and Methods 2.1. Identification and Characterization of HDAC Family in B. rapa Phytozome v12.1 (https://phytozome.jgi.doe.gov; Brassica rapa FPsc v1.3) was used to identify HDACs in B. rapa genome using BLASTp with Arabidopsis HDACs as queries. The conserved domains, molecular weight, phylogenetic, and isoelectric point (pI) analyses and subcellular localization of putative BraHDACs has been conducted by Eom and Hyun [21]. A nomenclature system for BraHDACs (generic name: BraHDA1 to 16 for the RPD3/HDA1 family, BraHDT1 and 2 for the HD2 family, and BraSRT1 and 2 for the SIR2 family) was used as described by Hollender and Liu [6]. 2.2. Gene Duplication and Calculating Duplication Times of BraHDAC Genes The Plant Genome Duplication Database (http://chibba.agtec.uga.edu/duplication/) was used to identify the homologous pairs among BraHDAC genes. Using PAL2NAL (http://www.bork.embl.de/pal2nal/), the synonymous rate (Ks), nonsynonymous rate (Ka), and evolutionary constraint (Ka/Ks) of duplicated BraHDAC genes were analyzed. −8 −6 The divergence time (T) was calculated using the formula T = Ks/(2 × 1.5 × 10 ) × 10 million years ago (MYA; [22]). 2.3. Plant Growth and Treatment Conditions Chinese cabbage (cultivar Chunkwang) seeds were grown in a growth chamber un‐ der long‐day conditions at 22 °C and 60% relative humidity. After 4 weeks, Chinese cab‐ bage plants were treated at 40 °C, and samples were harvested at the times indicated in Figure 2. Heat treatment was carried out three times, resulting in three biological repli‐ cates. Agriculture 2021, 11, 244 3 of 10 2.4. The Analysis of BraHDAC Expression Total RNA was extracted, quantified, and qualified using nanodrop. cDNA was syn‐ thesized using ReverTra Ace qPCR RT Master Mix with gDNA Remover. Quantitative RT‐PCR (qRT‐PCR) was performed using the SYBR Green Real‐time PCR Master Mix. The expression levels of each gene were normalized to the internal reference gene actin, and then was expressed relative to its value at 0 h. The specific primer pairs were designed using GenScript Real‐time PCR Primer Design tool, and are listed in Table S1. 2.5. Production of Recombinant BraHDA3 in E.coli, and the Analysis of HDAC Activity The PCR product of BraHDA3 was ligated into the pCR‐Blunt, and subcloned into the Escherichia coli expression vector pPROEX‐Htb vector that produces a histidine‐fused translation product. To produce his tagged‐BraHDA3 fusion proteins, E.coli strain BL21 harboring pPROEX‐BraHDA3 plasmid was incubated at 37 °C. Once the optical density at 600 nm reached 0.5, fusion proteins were produced by 0.1 mM isopropyl β‐ d‐1‐thio‐ galactopyranoside (IPTG) treatment for 16 h at 30 °C. The fusion protein was purified using Ni‐NTA affinity purification, and the HDAC activity was determined using HDAC Activity Colorimetric Assay Kit (BioVision, Milpitas, CA, USA). HDAC activity was cal‐ culated based on a standard curve generated with Ac‐Lys‐pNA (deacetylated standard). 2.6. Statistical Analyses The experimental results are expressed as means ± SE. SPSS Statistics version 25 (IBM Microsoft, New York, NY, USA) was used to carry out statistical analyses (Duncan multi‐ ple range tests). P values < 0.05 were regarded as statistically significant difference. 3. Results and Discussion 3.1. Identification of Histone Deacetylases in Chinese Cabbage Since HDACs have been introduced as erasers of epigenetic acetylation marks on lysine residues in histones, a number of plant HDAC genes have been identified from a variety of plant species [3]. From the B. rapa genome, we identified 20 HDAC members (Table 1). Among them, BraHDA6 was the largest protein, with 651 amino acids (AA), whereas BraHDA1 was identified as the smallest protein with 254 AA. The molecular weight of BraHDACs varied according to protein size, ranging from 28.8 KDa to 72.1 KDa, and their pI varied from 4.52 (BraHDT2) to 8.96 (BraSRT1). Subcellular locations as pre‐ dicted by WoLF PSORT indicated that BraHDACs were potentially localized in the cyto‐ sol, nucleus, chloroplast, mitochondria, and peroxisome (Table 1). Similar to the Arabidop‐ sis and soybean HD2 proteins [23,24], the B. rapa HD2 family were predicted as nuclear proteins (Table 1). In addition, BraSRT1 and BraSRT2 appeared to be localized in the mi‐ tochondria and nucleus, respectively, similar to the rice SRT (silent information regulator) family [25]. Taken together, the various localization patterns of BraHDACs indicated that they may have distinct roles. Plant RPD3/HDA1, HD2, and SIR2 families have been characterized by the presence of conserved domains such as the Hist_deacetyl domain (PF00850), SIR2 domain (PF02146), and ZnF_C2H2 domain (SM000355) [11,12]. As shown in Figure 1A, BraHDACs were divided into three major classes: RPD3/HDA1, HD2, and SIR2 families. The B. rapa genome encodes 16 proteins (Figures 1 and S1) clustered in the RPD3/HDA1 family contained the conserved Hist_deacetyl domain. In addition, two SIR2 family HDACs with highly conserved SIR2 domain and two HD2 family HDACs with conserved zinc finger C2H2 type domain (ZnF_C2H2) were identified. Another type of zinc finger domain, ZnF_RTZ (SM000547), has been found in BraHDA07, indicating that BraHDT1, BraHDT1, and BraHDA07 have high binding affinity to DNA or modulate protein‐protein interactions mediated by zinc finger domains [26]. The presence of domains similar to those in other plant HDACs suggested that all putative BraHDACs belong to the histone deacetylase family. Agriculture 2021, 11, 244 4 of 10 Figure 1. Phylogenetic tree, domain architectures (A) and synteny analysis (B) of the Brassica rapa HDAC family. Using the neighbor‐joining method, phylogenetic tree was generated. The conserved domains in the putative BraHDACs were analyzed with the SMART program. Paralogous gene pairs were analyzed using plant genome duplication database. Table 1. Histone deacetylase gene family in Brassica rapa. Subcellular Localiza‐ Name Gene ID Location CDS (bp) AA Intron Nr. pI kDa tion BraHDA1 Brara.A02927.1 A01:24968034..24970355 765 254 7 4.98 28.8 Cytosol BraHDA2 Brara.A03767.1 A01:29972774..29976555 1509 502 5 5.17 56.0 Nucleus BraHDA3 Brara.A00453.1 A01:2203688..2206445 1278 425 8 6.06 45.9 Chloroplast BraHDA4 Brara.B03745.1 A02:30976246..30978653 1668 555 8 5.93 62.0 Cytosol BraHDA5 Brara.C03690.1 A03:19011956..19014935 1797 598 13 6.00 65.8 Nucleus BraHDA6 Brara.C04226.1 A03:22262637..22266032 1956 651 12 5.23 72.1 Cytosol BraHDA7 Brara.E02343.1 A05:21170590..21174613 1638 545 16 5.60 59.8 Nucleus BraHDA8 Brara.F01687.1 A06:10370998..10372699 1230 409 4 4.97 45.4 Cytosol BraHDA9 Brara.F01690.1 A06:10386796..10389169 1200 399 4 5.82 44.4 Cytosol BraHDA10 Brara.F01971.1 A06:14950658..14953055 1272 423 4 8.70 47.6 Mitochondrial BraHDA11 Brara.F02002.1 A06:16050873..16053859 1281 426 13 5.32 48.7 Cytosol BraHDA12 Brara.F02210.1 A06:18915988..18918237 921 306 4 4.96 34.3 Nucleus BraHDA13 Brara.F02773.1 A06:22749037..22751166 1119 372 9 6.17 42.0 Cytosol BraHDA14 Brara.I00647.1 A09:3621688..3625470 1959 652 12 5.32 71.5 Peroxisome BraHDA15 Brara.I00727.1 A09:4109663..4112303 1413 470 5 4.94 52.7 Nucleus BraHDA16 Brara.I05307.1 A09:43269577..43271821 1161 386 2 5.68 42.2 Cytosol BraHDT1 Brara.A02332.1 A01:17662954..17671061 786 261 7 6.52 28.0 Nucleus BraHDT2 Brara.J02801.1 A10:19273043..19274967 858 285 6 4.52 31.2 Nucleus BraSRT1 Brara.B00303.1 A02:1417334..1419795 1047 357 8 8.96 39.7 Mitochondrial BraSRT2 Brara.C01390.1 A03:6592244..6595515 1407 468 13 6.49 52.4 Nucleus Agriculture 2021, 11, 244 5 of 10 3.2. Gene Duplication Analysis of BraHDACs Gene duplication has long been regarded as a key evolutionary process for acquiring new genes and genetic novelty [27]. It could occur on any of these scales: whole genome duplication, segmental duplication, and single gene duplication including tandem dupli‐ cation [28]. It has been shown that some HDACs expanded in the Gossypium and soybean genomes partly because of segmental duplication events [12,24]. In the B. rapa genome, 20 BraHDACs were asymmetrically distributed on 7 chromosomes (Table 1). Chromosome A06 contains the highest density of HDACs with six members (BraHDA8 to 13), followed by chromosome A01 with four genes (BraHDA1 to 3, BraSRT1), whereas only one BraHDAC was present on chromosome A05 (Table 1). A tandem duplication is character‐ ized as two or more adjacent homologous genes located physically “close” to one another; tandem duplicated pairs are paralogous genes on the same chromosome within a 50 kb physical distance [29], indicating that only one set (BraHDA8 and 9) was tandemly dupli‐ cated on chromosome A06 separated by 14,097 bp (Table 1) with 85.7% and 75.4% of se‐ quence identity at the nucleotide and protein levels. To further determine whether seg‐ mental duplication events also contributed to the expansion of BraHDACs, we analyzed the PGDD database combined with phylogenetic analysis. As shown in Figure 1B, seven duplicated BraHDAC gene pairs were identified, indicating that segmental duplication is a major contributory event leading to the expansion of BraHDAC genes in B. rapa genome. The highest frequency of segmental duplication events occurred between chromosomes A06 and 09, which contained two segmentally duplicated gene pairs. To examine the evolutionary selection process of eight duplicated gene pairs in B. rapa genome, we analyzed the evolutionary constraint (Ka/Ks). Ka/Ks ratios ranged from 0.0895 to 0.8713, and the average Ka/Ks value of the duplicated gene pairs was 0.404 (Table 2). This indicates that these duplicated gene pairs were subjected to negative selection (purifying selection), similar to duplicated HDAC gene pairs in Gossypium and soybean genomes [12,24]. The segmental duplications of HDAC genes in B. rapa genome occurred between 12.73 MYA and 42.04 MYA, with the average value being 29.19 MYA. The Ks of tandem duplications of BraHDAC genes was 0.1640, dating the duplication event at 5.47 MYA (Table 2). Brassicaceae, including Arabidopsis and Brassica, have been shown to have undergone three rounds of whole genome duplication, including γ triplication (135 MYA) and β (90–100 MYA) and α (24–40 MYA) duplications [30–32]. In addition, B. rapa exhibits this complex history, with the addition of a whole‐genome triplication occurring between 13 and 17 MYA [33], indicating that the segmental duplications of BraHDAC genes, except BraHDA 5/7 and BraHDA 12/15 gene pairs, occurred before whole‐genome triplication of the Brassica genome. Table 2. Divergence between paralogous histone acetyltransferase gene pairs in Brassica rapa. Gene 1 Gene 2 S N Ks Ka Ka/Ks Mya BraHDA8 BraHDA9 298.2 898.8 0.1640 0.1429 0.8713 5.47 BraHDA1 BraHDA5 176.0 574.0 1.2612 0.6244 0.4951 42.04 BraHDA1 BraHDA7 165.2 545.8 1.2066 0.4168 0.3454 40.22 BraHDA4 BraHDA6 371.3 1194.7 0.8011 0.3165 0.3951 26.70 BraHDA4 BraHDA14 399.2 1229.8 0.8870 0.3867 0.4360 29.57 BraHDA5 BraHDA7 319.5 925.5 0.4043 0.1344 0.3324 13.48 BraHDA15 BraHDA8 302.9 906.1 1.1871 0.3172 0.2672 39.57 BraHDA15 BraHDA12 215.5 693.5 0.3818 0.0342 0.0895 12.73 3.3. Effects of Heat Stress on Acetylation Status of Histone H3 in Chinese Cabbage Heat stress induces excessive generation of reactive oxygen species, resulting in al‐ terations in plant growth, development, photosynthesis, physiological processes, and pro‐ duction yield [34]. To evaluate the efficacy of heat treatment (40 °C), the physiological Agriculture 2021, 11, 244 6 of 10 response of Chinese cabbage including lipid peroxidation and proline content was ana‐ lyzed. As shown in Figure 2A, heat stress induced the accumulation of malondialdehyde (MDA), which is an indicator of lipid peroxidation [35]. In higher plants, the accumulation of proline, an amino acid and a compatible solute, is a common phenomenon in response to various environmental stresses [36]. We observed an increase in proline levels in re‐ sponse to heat stress (Figure 2B). The accumulated proline purportedly acts as a compat‐ ible osmolyte, molecular chaperone, cytosolic pH buffer, cell redox balancer, free radical scavenger, and stabilizer for subcellular structures during various stresses, especially os‐ motic and salt stresses [36,37], and improves resistance to various stresses [38]. However, proline accumulation in response to heat stress leads to increased production of reactive oxygen species in the mitochondria and inhibits ABA and ethylene biosynthesis, resulting in increased sensitivity to heat stress [36]. Taken together, these physiological changes suggested that the heat stress treatment was effective, and the leaves of heat‐treated plants were harvested for further analyses. To gain insight into the possible involvement of BraHDACs during their response to heat stress, the expression profiles of BraHDACs were analyzed. As shown in Figure 2C, exposure of Chinese cabbage plants to heat stress induced or repressed the expression of BraHDACs. After 48‐h exposure to heat stress, expression levels of BraHDA2, BraHDA4, BraHDA5, BraHDA6, BraHDA7, BraHDA11, BraHDA12, BraHDA15, BraHDA16, BraHDT2, and BraSRT2 had increased, whereas those of other BraHDACs decreased, remained un‐ changed, or were undetected. In addition, the transcript level of BraHDA13, BraHDA15, BraHDA16, BraHDT2, and BraSRT2 was up‐regulated in response to drought, salt, and wounding, whereas the decreasing level of BraHDA2, BraHDA3, BraHDA9, and BraHDA14 transcripts was observed (Figure S2). Under heat‐stress condition, BraHDA4 and BraHDA14 exhibited a different expression pattern, although BraHDA4 and BraHDA14 were clustered into same sub‐group in RPD3/HDA1 family, indicating that the duplication of those genes resulted in divergence of their expression pattern and function. Similar with BraHDACs, several Arabidopsis HDACs and maize HDACs in the class II of RPD3/HDA1 family were induced by heat treatment [11,39]. In addition, Arabidopsis, maize and cotton HDACs were differentially expressed in response to hormones and stresses, suggesting the functional divergence and specific regulation of HDACs in re‐ sponse to a particular stress [11,12,39]. According to the abiotic stress induced expression pattern of BraHDACs, we found that BraHDA8 was not expressed in leaves and on abiotic stresses. Based on transcriptome analysis, transcript level of BraHDA8 has been detected only in the silique [40], indicating that BraHDA8 should be expressed in specific tissue. In addition, the expression pattern of paralogous gene pair (BraHDA4/14) diverged, whereas three paralogous gene pairs (BraHDA4/6, BraHDA5/7, and BraHDA12/15) exhibited simi‐ lar expression patterns (Figure 2C) under heat stress condition. However, these expression patterns were altered in response to different stresses including drought, salt, and wound‐ ing (Figure S2), indicating that BraHDACs had diversified substantially, which might be due to the different divergent fates after duplications. Agriculture 2021, 11, 244 7 of 10 Figure 2. Physiological response to heat stress in Chinese cabbage. Changes in malondialdehyde (A) and proline (B) levels after exposure to heat stress (40 °C) were determined. (C) Expression patterns of Brassica rapa histone deacetylases (BraHDACs) in response to heat stress. Expression is indicated as a log2 ratio of experimental treatments relative to the values at 0 h. The bars represent the mean ± standard error across three independent experiments. Different letters indicate statistically signif‐ icant differences (p < 0.05). 3.4. Histone Deacetylase Activity of BarHDA3 Although many fundamental questions remain unanswered regarding the physio‐ logical function of plant HDACs in response to environmental stresses, it has been shown that RPD3/HDA1 family including Arabidopsis HDA5/14/15/18/19 positively or nega‐ tively regulated to the environmental‐stress tolerances [41]. Among them, AtHDA14 con‐ trolled the activation state of RuBisCO under low‐light condition, and is involved in bio‐ synthesis of melatonin, which plays an important role in plant response to environmental stresses [42,43]. Under heat stress condition, exogenous melatonin improved the antioxi‐ dant defense systems, resulting in the suppression of heat stress‐induced damage [44]. In Chinese cabbage, BraHDA3, homologous of AtHDA14 (Figure S1), dramatically down‐ regulated in response to heat stress (Figure 2C). This indicates that down‐regulation of BraHDA3 might be required for the expression of heat response genes, although the phys‐ iological function of BraHDA3 needs to be characterized. To analyze the function of BraHDA3, recombinant BraHDA3 (BraHDA3‐His) was prepared using E. coli expression system. As shown in Figure 3, purified recombinant BraHDA3 protein gave an activity of 18.1 μM/100 μg of protein. When HDAC inhibitor SAHA (5 μM) was mixed with purified recombinant BraHDA3 protein, the HDAC activity decreased to 3.8 μM/100 μg of protein. This indicates that BraHDA3 encodes the functional HDAC enzyme, which can be inhib‐ ited by Class I/II HDAC inhibitor SAHA. Agriculture 2021, 11, 244 8 of 10 Figure 3. HDAC activity of recombinant BraHDA3. SDS‐PAGE exhibited the purified recombinant BraHDA3 proteins. BraHDA3 enzyme activity was analyzed using HDAC Activity Colorimetric Assay Kit. Different letters indicate statistically significant differences (p < 0.05). 4. Conclusions Despite the knowledge concerning HDACs, evolutionary and functional information regarding HDACs in B. rapa remains relatively unknown. In this study, we identified 20 putative BraHDAC genes divided into three major classes: RPD3/HDA1, HD2, and SIR2 families. Most HDAC gene duplications in B. rapa appeared to have been caused by seg‐ mental duplication, which occurred between 12.73 MYA and 42.04 MYA. Several BraHDACs were up‐ or down‐regulated by abiotic stress treatments, indicating that the variation of BraHDAC transcription levels may contribute to alteration in histone H3 acet‐ ylation levels in response to various stresses. Our results provide a solid foundation for further understanding of the underlying evolutionary mechanisms in the HDAC family and will provide the basis for future research on functional characterization of the BraHDAC family in response to environmental stresses. Supplementary Materials: The following are available online at www.mdpi.com/2077‐ 0472/11/3/244/s1, Table S1: Primer sequences for PCR analysis, Figure S1. Phylogenetic relationships of Arabidopsis, maize, and Brassica rapa HDACs, Figure S2: Expression pattern of BraHDAC genes in response to wounding, salt, and drought stresses. Author Contributions: Conceptualization, S.H.E. and T.K.H.; investigation, S.H.E.; writing—origi‐ nal draft preparation, S.H.E. and T.K.H.; writing—review and editing, S.H.E. and T.K.H. All authors have read and agreed to the published version of the manuscript. Funding: This work was carried out with the support of “Cooperative Research Program for Agri‐ culture Science and Technology Development (Project No. PJ01501905)” Rural Development Ad‐ ministration, Republic of Korea. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. 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Agriculture – Multidisciplinary Digital Publishing Institute
Published: Mar 12, 2021
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