Top-down mass spectrometry of histone modifications in sorghum reveals potential epigenetic markers for drought acclimation

Zhou, Mowei; Malhan, Neha; Ahkami, Amir H.; Engbrecht, Kristin; Myers, Gabriel; Dahlberg, Jeffery; Hollingsworth, Joy; Sievert, Julie A.; Hutmacher, Robert; Madera, Mary; Lemaux, Peggy G.; Hixson, Kim K.; Jansson, Christer; Paša-Tolić, Ljiljana

doi:10.1016/j.ymeth.2019.10.007

Title: Top-down mass spectrometry of histone modifications in sorghum reveals potential epigenetic markers for drought acclimation

Journal Article · 22 October 2019 · Methods

DOI: https://doi.org/10.1016/j.ymeth.2019.10.007 · OSTI ID:1660761

^[1]; Malhan, Neha ^[2]; Ahkami, Amir H. ^[2]; Engbrecht, Kristin ^[2]; Myers, Gabriel ^[2]; Dahlberg, Jeffery ^[3]; Hollingsworth, Joy ^[3]; Sievert, Julie A. ^[3]; Hutmacher, Robert ^[4]; Madera, Mary ^[5]; Lemaux, Peggy G. ^[5]; Hixson, Kim K. ^[2]; Jansson, Christer ^[2]; Paša-Tolić, Ljiljana ^[2]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); Pacific Northwest National Laboratory
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
UC-ANR Kearney Agricultural Research & Extension Center, Parlier, CA (United States)
Univ. of California, Davis, CA (United States)
Univ. of California, Berkeley, CA (United States)

Sorghum [Sorghum bicolor (L.) Moench] is an important cereal crop noted for its ability to survive water-limiting conditions. In this paper, we present an analytical workflow to explore the changes in histone modifications through plant developmental stages and two drought stresses in two sorghum genotypes that differ in their response to drought. Top-down mass spectrometry (MS) is an ideal method to profile histone modifications and distinguish closely related histone proteoforms. We analyzed leaves of 48 plants and identified 26 unique histone proteins and 677 unique histone proteoforms (124 full-length and 553 truncated proteoforms). We detected trimethylation on nearly all H2B N-termini where acetylation is commonly expected. In addition, an unexpected modification on H2A histones was assigned to N-pyruvic acid 2-iminylation based on its unique neutral loss of CO₂. Interestingly, some of the truncated histones, in particular H4 and H3.2, showed significant changes that correlated with the growth and water conditions. Furthermore, the histone proteoforms could serve as targets in search of chromatin modifiers and ultimately have important ramifications in future attempts of studying plant epigenetic reprogramming under stress.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); University of California, Berkeley, CA (United States); Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA

Grant/Contract Number:: SC0014081; AC02-05CH11231

OSTI ID:: 1660761

Alternate ID(s):: OSTI ID: 1809705; OSTI ID: 1773357

Journal Information:: Methods, Journal Name: Methods Journal Issue: SI Vol. 184; ISSN 1046-2023

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (83)

Are neutral loss and internal product ions useful for top-down protein identification? Xiao, Kaijie; Yu, Fan; Fang, Houqin Journal of Proteomics, Vol. 160 https://doi.org/10.1016/j.jprot.2017.03.011	journal	May 2017
Quantitative Proteomic Analysis of Histone Modifications Huang, He; Lin, Shu; Garcia, Benjamin A. Chemical Reviews, Vol. 115, Issue 6 https://doi.org/10.1021/cr500491u	journal	October 2014
Unabridged Analysis of Human Histone H3 by Differential Top-Down Mass Spectrometry Reveals Hypermethylated Proteoforms from MMSET/NSD2 Overexpression Zheng, Yupeng; Fornelli, Luca; Compton, Philip D. Molecular & Cellular Proteomics, Vol. 15, Issue 3 https://doi.org/10.1074/mcp.M115.053819	journal	March 2016
The double face of the histone variant H3.3 Szenker, Emmanuelle; Ray-Gallet, Dominique; Almouzni, Geneviève Cell Research, Vol. 21, Issue 3 https://doi.org/10.1038/cr.2011.14	journal	January 2011
Characterization of Post-Translational Modifications of Histone H2B-Variants Isolated from Arabidopsis thaliana Bergmüller, Eveline; Gehrig, Peter M.; Gruissem, Wilhelm Journal of Proteome Research, Vol. 6, Issue 9 https://doi.org/10.1021/pr0702159	journal	September 2007
Top-down quantitation and characterization of SILAC-labeled proteins Waanders, Leonie F.; Hanke, Stefan; Mann, Matthias Journal of the American Society for Mass Spectrometry, Vol. 18, Issue 11 https://doi.org/10.1016/j.jasms.2007.09.001	journal	November 2007
iTop-Q: an Intelligent Tool for Top-down Proteomics Quantitation Using DYAMOND Algorithm Chang, Hui-Yin; Chen, Ching-Tai; Ko, Chu-Ling Analytical Chemistry, Vol. 89, Issue 24 https://doi.org/10.1021/acs.analchem.7b02343	journal	December 2017
Top-Down Proteomics of Large Proteins up to 223 kDa Enabled by Serial Size Exclusion Chromatography Strategy Cai, Wenxuan; Tucholski, Trisha; Chen, Bifan Analytical Chemistry, Vol. 89, Issue 10 https://doi.org/10.1021/acs.analchem.7b00380	journal	April 2017
Top-down/Bottom-up Mass Spectrometry Workflow Using Dissolvable Polyacrylamide Gels Takemori, Nobuaki; Takemori, Ayako; Wongkongkathep, Piriya Analytical Chemistry, Vol. 89, Issue 16 https://doi.org/10.1021/acs.analchem.7b00357	journal	July 2017
Informed-Proteomics: open-source software package for top-down proteomics Park, Jungkap; Piehowski, Paul D.; Wilkins, Christopher Nature Methods, Vol. 14, Issue 9 https://doi.org/10.1038/nmeth.4388	journal	August 2017
Regulation of nucleosome dynamics by histone modifications Zentner, Gabriel E.; Henikoff, Steven Nature Structural & Molecular Biology, Vol. 20, Issue 3 https://doi.org/10.1038/nsmb.2470	journal	March 2013
Progress in Top-Down Proteomics and the Analysis of Proteoforms Toby, Timothy K.; Fornelli, Luca; Kelleher, Neil L. Annual Review of Analytical Chemistry, Vol. 9, Issue 1 https://doi.org/10.1146/annurev-anchem-071015-041550	journal	June 2016
Top-down protein identification using isotopic envelope fingerprinting Xiao, Kaijie; Yu, Fan; Tian, Zhixin Journal of Proteomics, Vol. 152 https://doi.org/10.1016/j.jprot.2016.10.010	journal	January 2017
Nucleosome Structure and Function McGinty, Robert K.; Tan, Song Chemical Reviews, Vol. 115, Issue 6 https://doi.org/10.1021/cr500373h	journal	October 2014
Multi-faceted quantitative proteomics analysis of histone H2B isoforms and their modifications Molden, Rosalynn C.; Bhanu, Natarajan V.; LeRoy, Gary Epigenetics & Chromatin, Vol. 8, Issue 1 https://doi.org/10.1186/s13072-015-0006-8	journal	April 2015
Proteolytic clipping of histone tails: the emerging role of histone proteases in regulation of various biological processes Azad, Gajendra Kumar; Tomar, Raghuvir S. Molecular Biology Reports, Vol. 41, Issue 5 https://doi.org/10.1007/s11033-014-3181-y	journal	January 2014
Histone Variant H3.3: A versatile H3 variant in health and in disease Xiong, Chaoyang; Wen, Zengqi; Li, Guohong Science China Life Sciences, Vol. 59, Issue 3 https://doi.org/10.1007/s11427-016-5006-9	journal	January 2016
N-terminal methylation of proteins: Structure, function and specificity Stock, Ann; Clarke, Steven; Clarke, Catherine FEBS Letters, Vol. 220, Issue 1 https://doi.org/10.1016/0014-5793(87)80866-9	journal	August 1987
The C-Score: A Bayesian Framework to Sharply Improve Proteoform Scoring in High-Throughput Top Down Proteomics LeDuc, Richard D.; Fellers, Ryan T.; Early, Bryan P. Journal of Proteome Research, Vol. 13, Issue 7 https://doi.org/10.1021/pr401277r	journal	June 2014
Histones and histone genes in higher plants: Structure and genomic organization Chabouté, M. E.; Chaubet, N.; Gigot, C. Biochimie, Vol. 75, Issue 7 https://doi.org/10.1016/0300-9084(93)90057-Y	journal	January 1993
Identification of Protein N-Terminal Methyltransferases in Yeast and Humans Webb, Kristofor J.; Lipson, Rebecca S.; Al-Hadid, Qais Biochemistry, Vol. 49, Issue 25 https://doi.org/10.1021/bi100428x	journal	June 2010
A Mixed Integer Linear Optimization Framework for the Identification and Quantification of Targeted Post-translational Modifications of Highly Modified Proteins Using Multiplexed Electron Transfer Dissociation Tandem Mass Spectrometry* DiMaggio, Peter A.; Young, Nicolas L.; Baliban, Richard C. Molecular & Cellular Proteomics, Vol. 8, Issue 11 https://doi.org/10.1074/mcp.M900144-MCP200	journal	November 2009
Analyses of Histone Proteoforms Using Front-end Electron Transfer Dissociation-enabled Orbitrap Instruments Anderson, Lissa C.; Karch, Kelly R.; Ugrin, Scott A. Molecular & Cellular Proteomics, Vol. 15, Issue 3 https://doi.org/10.1074/mcp.O115.053843	journal	March 2016
N-terminal modifications of cellular proteins: The enzymes involved, their substrate specificities and biological effects Varland, Sylvia; Osberg, Camilla; Arnesen, Thomas PROTEOMICS, Vol. 15, Issue 14 https://doi.org/10.1002/pmic.201400619	journal	June 2015
Structural Diversity of Nucleosomes Characterized by Native Mass Spectrometry Saikusa, Kazumi; Osakabe, Akihisa; Kato, Daiki Analytical Chemistry, Vol. 90, Issue 13 https://doi.org/10.1021/acs.analchem.8b01649	journal	May 2018
Structure of the human adult hemoglobin minor fraction A1b by electrospray and secondary ion mass spectrometry. Pyruvic acid as amino-terminal blocking group Prome, D.; Blouquit, Y.; Ponthus, C. Journal of Biological Chemistry, Vol. 266, Issue 20 https://doi.org/10.1016/S0021-9258(18)98801-0	journal	July 1991
A Conserved Patch near the C Terminus of Histone H4 Is Required for Genome Stability in Budding Yeast Yu, Y.; Srinivasan, M.; Nakanishi, S. Molecular and Cellular Biology, Vol. 31, Issue 11 https://doi.org/10.1128/MCB.01432-10	journal	March 2011
Understanding the complex nature of salinity and drought-stress response in cereals using proteomics technologies Ngara, Rudo; Ndimba, Bongani K. PROTEOMICS, Vol. 14, Issue 4-5 https://doi.org/10.1002/pmic.201300351	journal	March 2014
Increasing the Separation Capacity of Intact Histone Proteoforms Chromatography Coupling Online Weak Cation Exchange-HILIC to Reversed Phase LC UVPD-HRMS Gargano, Andrea F. G.; Shaw, Jared B.; Zhou, Mowei Journal of Proteome Research, Vol. 17, Issue 11 https://doi.org/10.1021/acs.jproteome.8b00458	journal	September 2018
Designing sorghum as a dedicated bioenergy feedstock Rooney, William L.; Blumenthal, Jürg; Bean, Brent Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 2 https://doi.org/10.1002/bbb.15	journal	October 2007
Targeting the cancer epigenome for therapy Jones, Peter A.; Issa, Jean-Pierre J.; Baylin, Stephen Nature Reviews Genetics, Vol. 17, Issue 10 https://doi.org/10.1038/nrg.2016.93	journal	September 2016
Water-use efficiency of sweet sorghum under water stress conditions Gas-exchange investigations at leaf and canopy scales Steduto, P.; Katerji, N.; Puertos-Molina, H. Field Crops Research, Vol. 54, Issue 2-3 https://doi.org/10.1016/S0378-4290(97)00050-6	journal	September 1997
Histone H3 variants and their potential role in indexing mammalian genomes: The "H3 barcode hypothesis" Hake, S. B.; Allis, C. D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 17 https://doi.org/10.1073/pnas.0600803103	journal	March 2006
pTop 1.0: A High-Accuracy and High-Efficiency Search Engine for Intact Protein Identification Sun, Rui-Xiang; Luo, Lan; Wu, Long Analytical Chemistry, Vol. 88, Issue 6 https://doi.org/10.1021/acs.analchem.5b03963	journal	February 2016
Heavy Sugar and Heavy Water Create Tunable Intact Protein Mass Increases for Quantitative Mass Spectrometry in Any Feed and Organism Quijada, Jeniffer V.; Schmitt, Nicholas D.; Salisbury, Joseph P. Analytical Chemistry, Vol. 88, Issue 22 https://doi.org/10.1021/acs.analchem.6b03234	journal	October 2016
Profiling of Histone Post-Translational Modifications in Mouse Brain with High-Resolution Top-Down Mass Spectrometry Zhou, Mowei; Paša-Tolić, Ljiljana; Stenoien, David L. Journal of Proteome Research, Vol. 16, Issue 2 https://doi.org/10.1021/acs.jproteome.6b00694	journal	December 2016
Molecular basis for histone N-terminal methylation by NRMT1 Wu, Ruoxi; Yue, Yuan; Zheng, Xiangdong Genes & Development, Vol. 29, Issue 22 https://doi.org/10.1101/gad.270926.115	journal	November 2015
Histone proteolysis: A proposal for categorization into ‘clipping’ and ‘degradation’: Prospects & Overviews Dhaenens, Maarten; Glibert, Pieter; Meert, Paulien BioEssays, Vol. 37, Issue 1 https://doi.org/10.1002/bies.201400118	journal	October 2014
Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation Shilatifard, Ali Current Opinion in Cell Biology, Vol. 20, Issue 3 https://doi.org/10.1016/j.ceb.2008.03.019	journal	June 2008
Strong succession in arbuscular mycorrhizal fungal communities Gao, Cheng; Montoya, Liliam; Xu, Ling The ISME Journal, Vol. 13, Issue 1 https://doi.org/10.1038/s41396-018-0264-0	journal	August 2018
The conformational flexibility of the C-terminus of histone H4 promotes histone octamer and nucleosome stability and yeast viability Chavez, Myrriah S.; Scorgie, Jean K.; Dennehey, Briana K. Epigenetics & Chromatin, Vol. 5, Issue 1 https://doi.org/10.1186/1756-8935-5-5	journal	January 2012
SnapShot: Histone Modifications Huang, He; Sabari, Benjamin R.; Garcia, Benjamin A. Cell, Vol. 159, Issue 2 https://doi.org/10.1016/j.cell.2014.09.037	journal	October 2014
Epigenetic Regulation in Plant Responses to the Environment Baulcombe, D. C.; Dean, C. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 9 https://doi.org/10.1101/cshperspect.a019471	journal	September 2014
The PRIDE database and related tools and resources in 2019: improving support for quantification data Perez-Riverol, Yasset; Csordas, Attila; Bai, Jingwen Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1106	journal	November 2018
A New Approach for Plant Proteomics Zabrouskov, Vlad; Giacomelli, Lisa; van Wijk, Klaas J. Molecular & Cellular Proteomics, Vol. 2, Issue 12 https://doi.org/10.1074/mcp.M300069-MCP200	journal	December 2003
Enhanced top-down characterization of histone post-translational modifications Tian, Zhixin; Tolić, Nikola; Zhao, Rui Genome Biology, Vol. 13, Issue 10 https://doi.org/10.1186/gb-2012-13-10-r86	journal	January 2012
Plant Proteases: From Phenotypes to Molecular Mechanisms van der Hoorn, Renier A. L. Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092835	journal	June 2008
Top-Down Identification and Quantification of Stable Isotope Labeled Proteins from Aspergillus flavus Using Online Nano-Flow Reversed-Phase Liquid Chromatography Coupled to a LTQ-FTICR Mass Spectrometer Collier, Timothy S.; Hawkridge, Adam M.; Georgianna, D. Ryan Analytical Chemistry, Vol. 80, Issue 13 https://doi.org/10.1021/ac800254z	journal	July 2008
Involvement of Histone Modifications in Plant Abiotic Stress Responses: Histone Modifications in Plant Abiotic Stress Responses Yuan, Lianyu; Liu, Xuncheng; Luo, Ming Journal of Integrative Plant Biology, Vol. 55, Issue 10 https://doi.org/10.1111/jipb.12060	journal	August 2013
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria Xu, Ling; Naylor, Dan; Dong, Zhaobin Proceedings of the National Academy of Sciences, Vol. 115, Issue 18 https://doi.org/10.1073/pnas.1717308115	journal	April 2018
Histone variants on the move: substrates for chromatin dynamics Talbert, Paul B.; Henikoff, Steven Nature Reviews Molecular Cell Biology, Vol. 18, Issue 2 https://doi.org/10.1038/nrm.2016.148	journal	December 2016
The First Identification of Lysine Malonylation Substrates and Its Regulatory Enzyme Peng, Chao; Lu, Zhike; Xie, Zhongyu Molecular & Cellular Proteomics, Vol. 10, Issue 12 https://doi.org/10.1074/mcp.M111.012658	journal	September 2011
Clipping of Flexible Tails of Histones H3 and H4 Affects the Structure and Dynamics of the Nucleosome Nurse, Nathan P.; Jimenez-Useche, Isabel; Smith, Ian Tad Biophysical Journal, Vol. 104, Issue 5 https://doi.org/10.1016/j.bpj.2013.01.019	journal	March 2013
Applying Label-Free Quantitation to Top Down Proteomics Ntai, Ioanna; Kim, Kyunggon; Fellers, Ryan T. Analytical Chemistry, Vol. 86, Issue 10 https://doi.org/10.1021/ac500395k	journal	May 2014
Lysine Succinylation and Lysine Malonylation in Histones Xie, Zhongyu; Dai, Junbiao; Dai, Lunzhi Molecular & Cellular Proteomics, Vol. 11, Issue 5 https://doi.org/10.1074/mcp.M111.015875	journal	March 2012
Analysis of Histones H3 and H4 Reveals Novel and Conserved Post-Translational Modifications in Sugarcane Moraes, Izabel; Yuan, Zuo-Fei; Liu, Shichong PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0134586	journal	July 2015
Histone H3 Glutathionylation in Proliferating Mammalian Cells Destabilizes Nucleosomal Structure García-Giménez, José Luis; Olaso, Gloria; Hake, Sandra B. Antioxidants & Redox Signaling, Vol. 19, Issue 12 https://doi.org/10.1089/ars.2012.5021	journal	October 2013
Identification of five sites of acetylation in alfalfa histone H4 Waterborg, Jakob H. Biochemistry, Vol. 31, Issue 27 https://doi.org/10.1021/bi00142a006	journal	July 1992
Mass Spectrometric Quantification of Histone Post-translational Modifications by a Hybrid Chemical Labeling Method Maile, Tobias M.; Izrael-Tomasevic, Anita; Cheung, Tommy Molecular & Cellular Proteomics, Vol. 14, Issue 4 https://doi.org/10.1074/mcp.O114.046573	journal	February 2015
An improved workflow for quantitative N-terminal charge-based fractional diagonal chromatography (ChaFRADIC) to study proteolytic events in Arabidopsis thaliana Venne, A. Saskia; Solari, Fiorella A.; Faden, Frederik PROTEOMICS, Vol. 15, Issue 14 https://doi.org/10.1002/pmic.201500014	journal	July 2015
Role of glutathione in the regulation of epigenetic mechanisms in disease García-Giménez, José Luis; Romá-Mateo, Carlos; Pérez-Machado, Gisselle Free Radical Biology and Medicine, Vol. 112 https://doi.org/10.1016/j.freeradbiomed.2017.07.008	journal	November 2017
N-Trimethylalanine, a Novel Blocked N-Terminal Residue of Tetrahymena Histone H2B1 Nomoto, Minoru; Kyogoku, Yoshimasa; Iwai, Koichi The Journal of Biochemistry, Vol. 92, Issue 5 https://doi.org/10.1093/oxfordjournals.jbchem.a134096	journal	October 1982
Characterization of Chlamydomonas reinhardtii Core Histones by Top-Down Mass Spectrometry Reveals Unique Algae-Specific Variants and Post-Translational Modifications Khan, Aliyya; Eikani, Carlo K.; Khan, Hana Journal of Proteome Research, Vol. 17, Issue 1 https://doi.org/10.1021/acs.jproteome.7b00780	journal	November 2017
Histones of Chlamydomonas reinhardtii (Synthesis, Acetylation, and Methylation) Waterborg, J. H.; Robertson, A. J.; Tatar, D. L. Plant Physiology, Vol. 109, Issue 2 https://doi.org/10.1104/pp.109.2.393	journal	October 1995
Identification and Quantification of Proteoforms by Mass Spectrometry Schaffer, Leah V.; Millikin, Robert J.; Miller, Rachel M. PROTEOMICS, Vol. 19, Issue 10 https://doi.org/10.1002/pmic.201800361	journal	May 2019
Genetic Engineering and Water Somerville, C. Science, Vol. 292, Issue 5525 https://doi.org/10.1126/science.292.5525.2217	journal	June 2001
Intact Protein Quantitation Using Pseudoisobaric Dimethyl Labeling Fang, Houqin; Xiao, Kaijie; Li, Yunhui Analytical Chemistry, Vol. 88, Issue 14 https://doi.org/10.1021/acs.analchem.6b01388	journal	July 2016
Using ChIP-Seq Technology to Generate High-Resolution Profiles of Histone Modifications O’Geen, Henriette; Echipare, Lorigail; Farnham, Peggy J. Methods in Molecular Biology https://doi.org/10.1007/978-1-61779-316-5_20	book	January 2011
Variations of Histone Modification Patterns: Contributions of Inter-plant Variability and Technical Factors Brabencová, Sylva; Ihnatová, Ivana; Potěšil, David Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02084	journal	December 2017
Tandem Mass Tag Protein Labeling for Top-Down Identification and Quantification Hung, Chien-Wen; Tholey, Andreas Analytical Chemistry, Vol. 84, Issue 1 https://doi.org/10.1021/ac202243r	journal	December 2011
Distinctive Core Histone Post-Translational Modification Patterns in Arabidopsis thaliana Zhang, Kangling; Sridhar, Vaniyambadi V.; Zhu, Jianhua PLoS ONE, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pone.0001210	journal	November 2007
Characterization of Tetrahymena Histone H2B Variants and Posttranslational Populations by Electron Capture Dissociation (ECD) Fourier Transform Ion Cyclotron Mass Spectrometry (FT-ICR MS) Medzihradszky, K. F.; Zhang, X.; Chalkley, R. J. Molecular & Cellular Proteomics, Vol. 3, Issue 9 https://doi.org/10.1074/mcp.M400041-MCP200	journal	September 2004
Drought under global warming: a review: Drought under global warming Dai, Aiguo Wiley Interdisciplinary Reviews: Climate Change, Vol. 2, Issue 1 https://doi.org/10.1002/wcc.81	journal	October 2010
Top-down high-resolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state Ge, Y.; Rybakova, I. N.; Xu, Q. Proceedings of the National Academy of Sciences, Vol. 106, Issue 31 https://doi.org/10.1073/pnas.0813369106	journal	June 2009
Native GELFrEE: A New Separation Technique for Biomolecular Assemblies Skinner, Owen S.; Do Vale, Luis H. F.; Catherman, Adam D. Analytical Chemistry, Vol. 87, Issue 5 https://doi.org/10.1021/ac504678d	journal	February 2015
Sorghum bicolor — an important species for comparative grass genomics and a source of beneficial genes for agriculture Mullet, John E.; Klein, Robert R.; Klein, Patricia E. Current Opinion in Plant Biology, Vol. 5, Issue 2 https://doi.org/10.1016/S1369-5266(02)00232-7	journal	April 2002
Decoding protein modifications using top-down mass spectrometry Siuti, Nertila; Kelleher, Neil L. Nature Methods, Vol. 4, Issue 10 https://doi.org/10.1038/nmeth1097	journal	September 2007
Protein N-terminal methionine excision Giglione, C.; Boularot, A.; Meinnel, T. Cellular and Molecular Life Sciences, Vol. 61, Issue 12 https://doi.org/10.1007/s00018-004-3466-8	journal	June 2004
MASH Suite Pro: A Comprehensive Software Tool for Top-Down Proteomics Cai, Wenxuan; Guner, Huseyin; Gregorich, Zachery R. Molecular & Cellular Proteomics, Vol. 15, Issue 2 https://doi.org/10.1074/mcp.O115.054387	journal	November 2015
The top-down, middle-down, and bottom-up mass spectrometry approaches for characterization of histone variants and their post-translational modifications Moradian, Annie; Kalli, Anastasia; Sweredoski, Michael J. PROTEOMICS, Vol. 14, Issue 4-5 https://doi.org/10.1002/pmic.201300256	journal	December 2013
Mass spectrometry analysis of the variants of histone H3 and H4 of soybean and their post-translational modifications Wu, Tao; Yuan, Tiezheng; Tsai, Sau-Na BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-98	journal	January 2009
Two-dimensional separation using high-pH and low-pH reversed phase liquid chromatography for top-down proteomics Wang, Zhe; Ma, Hongyan; Smith, Kenneth International Journal of Mass Spectrometry, Vol. 427 https://doi.org/10.1016/j.ijms.2017.09.001	journal	April 2018
Top-down and Middle-down Protein Analysis Reveals that Intact and Clipped Human Histones Differ in Post-translational Modification Patterns* Tvardovskiy, Andrey; Wrzesinski, Krzysztof; Sidoli, Simone Molecular & Cellular Proteomics, Vol. 14, Issue 12 https://doi.org/10.1074/mcp.M115.048975	journal	December 2015

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59 BASIC BIOLOGICAL SCIENCES
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Sorghum
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Title: Top-down mass spectrometry of histone modifications in sorghum reveals potential epigenetic markers for drought acclimation

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