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Acetylproteomics analyses reveal critical features of lysine-ε-acetylation in Arabidopsis and a role of 14-3-3 protein acetylation in alkaline response

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Stress Biology 2022年第1期2卷 685-703页

作者： Jianfei Guo Xiaoqiang Chai Yuchao Mei Jiamu Du Haining Du Huazhong Shi Jian-Kang Zhu Heng Zhang State Key Laboratory of Plant Molecular Genetics Shanghai Center for Plant Stress BiologyCenter for Excellence in Plant Molecular SciencesChinese Academy of SciencesShanghai 201602China University of Chinese Academy of Sciences Beijing 100049China Hubei Key Laboratory of Cell Homeostasis College of Life SciencesWuhan UniversityWuhan 430072China Department of Biology Institute of Plant and Food ScienceSouthern University of Science and TechnologyShenzhen 518055GuangdongChina Department of Chemistry and Biochemistry Texas Tech UniversityLubbockTXUSA

lysine-ε-acetylation(Kac)is a post-translational modification(PTM)that is critical for metabolic regulation and cell signaling in mammals.However,its prevalence and importance in plants remain to be determined.Employing high-resolution tandem mass spectrometry,we analyzed protein lysine acetylation in five representative Arabidopsis organs with 2~3 biological replicates per organ.A total of 2887 Kac proteins and 5929 Kac sites were identified.This comprehensive catalog allows us to analyze proteome-wide features of lysine acetylation.We found that Kac proteins tend to be more uniformly expressed in different organs,and the acetylation status exhibits little correlation with the gene expression level,indicating that acetylation is unlikely caused by stochastic processes.Kac preferentially targets evolutionarily conserved proteins and lysine residues,but only a small percentage of Kac proteins are orthologous between rat and Arabidopsis.A large portion of Kac proteins overlap with proteins modified by other PTMs including ubiquitination,SUMOylation and phosphorylation.Although acetylation,ubiquitination and SUMOylation all modify lysine residues,our analyses show that they rarely target the same sites.In addition,we found that“reader”proteins for acetylation and phosphorylation,i.e.,bromodomain-containing proteins and GRF(General Regulatory Factor)/14-3-3 proteins,are intensively modified by the two PTMs,suggesting that they are main crosstalk nodes between acetylation and phosphorylation signaling.Analyses of GRF6/14-3-3λreveal that the Kac level of GRF6 is decreased under alkaline stress,suggesting that acetylation represses plant alkaline response.Indeed,K56ac of GRF6 inhibits its binding to and subsequent activation of the plasma membrane H+-ATPase AHA2,leading to hypersensitivity to alkaline stress.These results provide valuable resources for protein acetylation studies in plants and reveal that protein acetylation suppresses phosphorylation output by acetylating GRF/14-3-3 proteins.

关键词： lysine acetylation Mass spectrometry PTM crosstalk 14-3-3 Alkaline stress

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An enhanced network of energy metabolism,lysine acetylation,and growth-promoting protein accumulation is associated with heterosis in elite hybrid rice

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Plant Communications 2023年第4期4卷 146-159页

作者： Xuan Ma Qingxiao Jia Sheng Li Zhengting Chen Xin Ming Yu Zhao Dao-Xiu Zhou National Key Laboratory of Crop Genetic Improvement Hubei Hongshan LaboratoryHuazhong Agricultural UniversityWuhan 430070China Institute of Plant Science Paris-Saclay(IPS2) CNRSINRAEUniversity Paris-Saclay91405 OrsayFrance

Heterosis refers to the superior performance of a hybrid compared with its parental lines.Although several genetic and molecular models have been proposed to explain heterosis,it remains unclear how hybrid cells integrate complementary gene expression or activity to drive heterotic growth.In this work,we show that accumulation of growth-promoting and energy metabolism proteins,enhanced energy metabolism activities,and increased protein lysine acetylation were associated with superior growth of the panicle meristem in the elite hybrid rice Shanyou 63 relative to its parental varieties.Metabolism of nuclear/cytosolic acetylcoenzyme A was also enhanced in the hybrid,which paralleled increases in histone H3 acetylation to selectively target the expression of growth-promoting and metabolic genes.lysine acetylation of cellular proteins,including TARGET OF RAPAMYCIN complex 1,ribosomal proteins,and energy metabolism enzymes,was also augmented and/or remodeled to modulate their activities.The data indicate that an enhanced network of energy-producing metabolic activity and growth-promoting histone acetylation/gene expression in the hybrid could contribute to its superior growth rate and may constitute a model to explain heterosis.

关键词： heterosis TORC1 r-protein lysine acetylation energy metabolism hybrid rice

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lysine acetylation decreases enzyme activity and protein level of Escherichia coli lactate dehydrogenase

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Engineering Microbiology 2022年第4期2卷 1-7页

作者： Min Liu Meitong Huo Likun Guo Yingxin Fu Mo Xian Qingsheng Qi Wei Liu Guang Zhao State Key Laboratory of Microbial Technology Shandong UniversityQingdao 266237China Institute of Corrosion Science and Technology Guangzhou 510530China CAS Key Laboratory of Biobased Materials Qingdao Institute of Bioenergy and Bioprocess TechnologyChinese Academy of SciencesQingdao 266101China

Lactate is an important bulk chemical with widespread applications and a major byproduct of other chemicals bioprocess in microbial fermentation.Lactate dehydrogenase A(LdhA)catalyzes the synthesis of lactate from pyruvate.lysine acetylation is an evolutionarily conserved post-translational modification;however,the mech-anisms underlying the regulation of LdhA function by lysine acetylation in Escherichia coli remain poorly under-stood.Herein,we demonstrate acetylation of E.coli LdhA occurs via enzymatic and non-enzymatic mechanisms.Further,we show carbon source type and concentration affect the lysine acetylation status of LdhA via a non-enzymatic mechanism.lysine acetylation significantly inhibits the enzymatic activity and protein level of LdhA.The results of the present study demonstrate lysine acetylation of E.coli LdhA is irreversible.Understanding of the effects of lysine acetylation on LdhA function may provide a new perspective for regulating lactate production in microbial synthesis.

关键词： lysine acetylation Lactate dehydrogenase A Lactate synthesis Protein degradation

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New lysine-acetylated proteins screened by immunoaffinity and liquid chromatography-mass spectrometry

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Science China Chemistry 2010年第1期53卷 238-244页

作者： ZHANG Bing ZHAO Chao LUO KaiXuan YAN GuoQuan YAO Jun WANG YingYin LU HaoJie FAN HuiZhi YANG PengYuan Department of Chemistry Fudan UniversityShanghai 200433China Institutes of Biomedical Sciences Fudan UniversityShanghai 200032China

The lack of selective extraction specific for lysine-acetylated proteins has been a major problem in the field of acetylation biology,though acetylation plays a key role in many biological processes.In this paper,we report for the first time the proteomic screening of lysine-acetylated proteins from a mouse liver tissue,by a new approach of immunoaffinity purification of lysine-acetylated peptides combined with nano-HPLC/MS/MS analysis.We have found 20 lysine-acetylated proteins with 21 lysine-acetylated sites,among which 12 lysine-acetylated proteins and 16 lysine-acetylated sites have never been reported before.Notably,three acetyltransferases harboring in mitochondrion are newly discovered acetyltransferases responsible for the acetylation of nonhistone proteins.We have explored the significant patterns of residue preference by the hierarchical clustering analysis of amino acid residues surrounding acetylation sites,which could be helpful to the prediction of new sites of lysine acetylation.Our findings provide more candidates for studying the important roles played by acetylation in diverse cellular pathways and related human diseases.

关键词： lysine acetylation immunoaffinity purification liquid chromatography mass spectrometry

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Proteomic Analysis of lysine acetylation in Magnaporthe oryzae

Proteomic Analysis of Lysine Acetylation in Magnaporthe oryz...

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中国菌物学会2015年学术年会

作者： Jinguang Huang Jun Yang Minfeng Xue Hengwei Qian Wenxing Liang You-Liang Peng College of Agronomy and Plant Protection Qingdao Agricultural University State key Laboratory of Agrobiotechnology MOA Key Laboratory of Plant PathologyChina Agricultrual University Institute of Plant Protection and Soil Science Hubei Academy of Agricultural Sciences

Magnaporthe oryzae, the causal agent of rice blast, has been used as a model for investigating the interaction between phytopathogenic fungi and plants. lysine acetylation is emerging as a ubiquitous and conserved posttranslational modificationin living cells. While the role of lysine acetylation in regulating primary metabolism is well-established, its function in secondary metabolism remains largely elusive. To gain insight into the nature, extent and biological function of lysine acetylation in M.oryzae, we used the combination of affinity enrichment and high-resolution LC-MS/MS analysis to perform large-scale lysine acetylome analysis. Altogether, 1,283 lysine acetylation sites in 738 protein groups were identified. Intensive bioinformatics analysis was then carried out to annotate those lysine acetylated targets, including protein annotation, functional classification, functional enrichment, functional enrichment-based cluster analysis, etc. Based on the results, further studies following the large-scale lysine acetylome analysis were suggested.

关键词： Magnaporthe oryzae Proteomic lysine acetylation

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Global Proteome Analyses of lysine acetylation in the Embryo of Germinating Wheat Seed

Global Proteome Analyses of Lysine Acetylation in the Embryo...

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第十届全国小麦基因组学及分子育种大会

作者： Weiwei Guo Liping Han Ximei Li Huifang Wang Ping Mu Qi Lin Qingchang Liu Yumei Zhang Shandong Provincial Key Laboratory of Dry Farming Technology/Shandong Engineering Research Center of Germplasm Innovation and Utilization of Salt-tolerant Crops College of Agronomy Qingdao Agricultural University Laboratory of Crop Heterosis and Utilization Ministry of EducationChina Agricultural University

Seed germination is the first stage for wheat growth and development,and this stage affects grain yield and quality directly.As an important post-translation modification,lysine acetylation participates in diverse biological functions.However,little is known regarding the quantitative acetylproteome characterization during wheat seed germination.In this study,we generated the first comparative proteomes and lysine acetylomes during seed germination.In total,5639 proteins and 1301 acetylated sites on 722 proteins were identified in both stages.Our results revealed that several particular preferred amino acids near acetylation sites,including KS,KT,KK,KR,KH,KF,KN,KE,FK and KD,were identified in the embryos during seed germination.Among them,KH,KF,FK and KK were conserved in wheat.We also revealed that the key enzyme CYP71 C8 v2 that catabolizes the ABA was up-regulated at the level of acetylation.Meanwhile,eight enzymes that played important roles in glycolysis and the TCA cycle,and some stress-related and ROS-scavenging proteins were also acetylated.In addition,a putative metabolic pathway was proposed to dissect the roles of protein acetylation during wheat seed germination.

关键词： Seed germination Post-translational modification lysine acetylation Acetylome Triticum aestivum L

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Proteomic analysis of lysine acetylation in Magnaporthe oryzae

Proteomic analysis of lysine acetylation in Magnaporthe oryz...

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中国植物病理学会第十二届青年学术研讨会

Magnaporthe oryzae,the causal agent of rice blast,has been used as a model for investigating the interaction between phytopathogenic fungi and plants.lysine acetylation is emerging as a ubiquitous and conserved posttranslational modificationin living cells.While the role of lysine acetylation in regulating primary metabolism is well-established,its function in secondary metabolism remains largely elusive.To gain insight into the nature,extent and biological function of lysine acetylation in M.oryzae,we used the combination of affinity enrichment and high-resolution LC-MS/MS analysis to perform large-scale lysine acetylome analysis.Altogether,1 283 lysine acetylation sites in 738 protein groups were identified.Intensive bioinformatics analysis was then carried out to annotate those lysine acetylated targets,including protein annotation,functional classification,functional enrichment,functional enrichmentbased cluster analysis,etc.Based on the results,further studies following the largescale lysine acetylome analysis are underway.

关键词： Magnaporthe oryzae proteomic lysine acetylation

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Global proteome analysis links lysine acetylation to diverse functions in Oryza sativa

Global proteome analysis links lysine acetylation to diverse...

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2017中国长三角遗传学大会

作者： Chao Xue Shuai Liu Chen Chen Xibin Yang Yong Zhou Rui Guo Xiaoyu Liu Zhiyun Gong Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops Key Laboratory of Plant Functional Genomics of the Ministry of EducationYangzhou University

lysine acetylation(Kac) is an important protein post-translational modification in both eukaryotes and prokaryotes.Herein,we report the results of a global proteome analysis of lysine acetylation and its diverse functions in rice[Oryza sativo).We identified 1353 Kac sites in 866 proteins in rice seedlings.A total of 11 Kac motifs are conserved,and 45%of the identified proteins are localised to the chloroplast.Among all acetylated proteins,38 Kac sites are combined in core histones.Bioinformatics analysis revealed that Kac occurs on a diverse range of proteins involved in a wide variety of biological processes,especially photosynthesis.Protein-protein interaction networks of the identified proteins provided further evidence that Kac contributes to a wide range of regulatory functions.Furthermore,we demonstrated that the acetylation level of histone H3(lysine 27 and 36) is increased in response to cold stress.In summary,our approach comprehensively profiles the regulatory roles of Kac in the growth and development of rice.

关键词： Oryza sativa lysine acetylation acetylome photosynthesis cold stress

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Histone Deacetylase AtSRT1 Links Metabolic Flux and Stress Response in Arabidopsis

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Molecular Plant 2017年第12期10卷 1510-1522页

作者： Xiaoyun Liu Wei Wei Wenjun Zhu Lufang Su Zeyang Xiong Man Zhou Yu Zheng and Dao-Xiu Zhou Institute for Interdisciplinary Research Jianghan University Wuhan 430056 China Institute Plant Science Paris-Saclay (IPS2) CNRS INRA Universite Paris-sud 11 Univeraite Paris-Saclay B630 91405 Orsay France College of Biology and Pharmaceutical Engineering Wuhan Polytechnic University Wuhan 430023 China These authors contributed equally to this article.

How plant metabolic flux alters gene expression to optimize plant growth and response to stress remains largely unclear. Here, we report that Arabidopsis thaliana NAD＊-dependent histone deacetylase AtSRT1 negatively regulates plant tolerance to stress and glycolysis but stimulates mitochondrial respiration. We found that AtSRT1 interacts with Arabidopsis cMyc-Binding Protein 1 （AtMBP-1）, a transcriptional repressor produced by alternative translation of the cytosolic glycolytic enolase gene LOS2/EN02. We demonstrated that AtSRT1 could associate with the chromatin of AtMBP-I targets LOS2/EN02 and STZ/ZATIO, both of which encode key stress regulators, and reduce the H3K9ac levels at these genes to repress their transcription. Overexpression of both AtSRT1 and AtMBP-1 had synergistic effects on the expression of glycolytic genes, glycolytic enzymatic activities, and mitochondrial respiration. Furthermore, we found that AtMBP-1 is lysine-acetylated and vulnerable to proteasomal protein degradation, while AtSRT1 could remove its lysine acetylation and significantly enhance its stability in vivo. Taken together, these results indicate that AtSRT1 regulates primary metabolism and stress response by both epigenetic regulation and modulation of AtMBP-1 transcriptional activity in Arabidopsis.

关键词： chromartin histone modification HDAC sirtuin lysine acetylation metabolism

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Histone Deacetylase HDA9 and WRKY53 Transcription Factor Are Mutual Antagonists in Regulation of Plant Stress Response

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Molecular Plant 2020年第4期13卷 598-611页

作者： Yu Zheng Jingyu Ge Chun Bao Wenwen Chang Jingjing Liu Jingjie Shao Xiaoyun Liu Lufang Su Lei Pan Dao-Xiu Zhou Institute for Interdisciplinary Research and Hubei Province Engineering Research Center of Legume Plants Jianghan UniversityWuhan 430056China Institute of Plant Sciences Paris-Saclay CNRSINRAEUniversite Paris-SaclayOrsay 91405France

Epigenetic regulation of gene expression is important for plant adaptation to environm ental changes.Previous results showed that Arabidopsis RPD3-like histone deacetylase HDA9 is known to function in repressing plant response to stress in Arabidopsis.However,how HDA9 targets to specific chromatin loci and controls gene expression netw orks involved in plant response to stress remains largely unclear.Here,we show that HDA9 represses stress tolerance response by interacting with and regulating the DNA binding and transcriptional activity of WRKY53,which functions as a high-hierarchy positive regulator of stress response.We found that WRKY53 is post-translationally modified by lysine acetylation at multiple sites,some of which are removed by HDA9,resulting in inhibition of WRKY53 transcription activity.Conversely,WRKY53 negatively regulates HDA9 histone deacetylase activity.Collectively,our results indicate that HDA9 and WRK53 are reciprocal negative regulators of each other's activities,illustrating how the functional interplay between a chromatin regulator and a transcription factor regulates stress tolerance in plants.

关键词： HDA9 WRKY53 stress lysine acetylation transcription activity

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