Two related families of metal transferases, ZNG1 and ZNG2, are involved in acclimation to poor Zn nutrition in Arabidopsis

Zhang, Lifang; Braynen, Janeen; Fahey, Audrey; Chopra, Kriti; Cifani, Paolo; Tadesse, Dimiru; Regulski, Michael; Hu, Fangle; van Dam, Hubertus J. J.; Xie, Meng; Ware, Doreen; Blaby-Haas, Crysten E.

doi:10.3389/fpls.2023.1237722

Two related families of metal transferases, ZNG1 and ZNG2, are involved in acclimation to poor Zn nutrition in Arabidopsis

Journal Article · Wed Oct 25 00:00:00 EDT 2023 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2023.1237722· OSTI ID:2267567

Zhang, Lifang ^[1]; Braynen, Janeen ^[1]; Fahey, Audrey ^[1]; Chopra, Kriti ^[2]; Cifani, Paolo ^[1]; Tadesse, Dimiru ^[2]; Regulski, Michael ^[1]; Hu, Fangle ^[1]; van Dam, Hubertus J. J. ^[2]; Xie, Meng ^[2]; Ware, Doreen ^[3]; Blaby-Haas, Crysten E. ^[4]

Cold Spring Harbor Laboratory, NY (United States)
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Cold Spring Harbor Laboratory, NY (United States); US Department of Agriculture (USDA), Ithaca, NY (United States). Agricultural Research Service (ARS), Robert W. Holley Research Center for Agriculture and Health (RHRC)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Molecular Foundry; Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). USDOE Joint Genome Institute (JGI)

Metal homeostasis has evolved to tightly modulate the availability of metals within the cell, avoiding cytotoxic interactions due to excess and protein inactivity due to deficiency. Even in the presence of homeostatic processes, however, low bioavailability of these essential metal nutrients in soils can negatively impact crop health and yield. While research has largely focused on how plants assimilate metals, acclimation to metal-limited environments requires a suite of strategies that are not necessarily involved in metal transport across membranes. The identification of these mechanisms provides a new opportunity to improve metal-use efficiency and develop plant foodstuffs with increased concentrations of bioavailable metal nutrients. Here, we investigate the function of two distinct subfamilies of the nucleotide-dependent metallochaperones (NMCs), named ZNG1 and ZNG2, that are found in plants, using Arabidopsis thaliana as a reference organism. AtZNG1 (AT1G26520) is an ortholog of human and fungal ZNG1, and like its previously characterized eukaryotic relatives, localizes to the cytosol and physically interacts with methionine aminopeptidase type I (AtMAP1A). Analysis of AtZNG1, AtMAP1A, AtMAP2A, and AtMAP2B transgenic mutants are consistent with the role of Arabidopsis ZNG1 as a Zn transferase for AtMAP1A, as previously described in yeast and zebrafish. Structural modeling reveals a flexible cysteine-rich loop that we hypothesize enables direct transfer of Zn from AtZNG1 to AtMAP1A during GTP hydrolysis. Based on proteomics and transcriptomics, loss of this ancient and conserved mechanism has pleiotropic consequences impacting the expression of hundreds of genes, including those involved in photosynthesis and vesicle transport. Members of the plant-specific family of NMCs, ZNG2A1 (AT1G80480) and ZNG2A2 (AT1G15730), are also required during Zn deficiency, but their target protein(s) remain to be discovered. In conclusion, RNA-seq analyses reveal wide-ranging impacts across the cell when the genes encoding these plastid-localized NMCs are disrupted.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0012704

OSTI ID:: 2267567

Alternate ID(s):: OSTI ID: 2440369

Report Number(s):: BNL--225097-2023-JAAM

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 14; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (97)

Probability-based protein identification by searching sequence databases using mass spectrometry data Perkins, David N.; Pappin, Darryl J. C.; Creasy, David M. Electrophoresis, Vol. 20, Issue 18 https://doi.org/10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2	journal	December 1999
Mapping RNA‐seq Reads with STAR Dobin, Alexander; Gingeras, Thomas R. Current Protocols in Bioinformatics, Vol. 51, Issue 1 https://doi.org/10.1002/0471250953.bi1114s51	journal	September 2015
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System Goddard, Thomas D.; Huang, Conrad C.; Meng, Elaine C. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/PRO.3235	journal	September 2017
Yeast methionine aminopeptidase I can utilize either Zn ²⁺ or Co ²⁺ as a cofactor: A case of mistaken identity? Walker, Kenneth W.; Bradshaw, Ralph A. Protein Science, Vol. 7, Issue 12 https://doi.org/10.1002/pro.5560071224	journal	December 1998
The Specificity in Vivo of Two Distinct Methionine Aminopeptidases in Saccharomyces cerevisiae Chen, Shaoping; Vetro, Joseph A.; Chang, Yie-Hwa Archives of Biochemistry and Biophysics, Vol. 398, Issue 1 https://doi.org/10.1006/abbi.2001.2675	journal	February 2002
Classification and evolution of P-loop GTPases and related ATPases Leipe, Detlef D.; Wolf, Yuri I.; Koonin, Eugene V. Journal of Molecular Biology, Vol. 317, Issue 1 https://doi.org/10.1006/jmbi.2001.5378	journal	March 2002
The use of cytoplasmic streptomycin resistance: Chloroplast transfer from Nicotiana tabacum into Nicotiana sylvestris, and Isolation of their somatic hybrids Medgyesy, Péter; Menczel, László; Maliga, Pál Molecular and General Genetics MGG, Vol. 179, Issue 3 https://doi.org/10.1007/BF00271759	journal	October 1980
Label-Free Proteomics of a Defined, Binary Co-culture Reveals Diversity of Competitive Responses Between Members of a Model Soil Microbial System Chignell, J. F.; Park, S.; Lacerda, C. M. R. Microbial Ecology, Vol. 75, Issue 3 https://doi.org/10.1007/s00248-017-1072-1	journal	October 2017
Emergence of metal selectivity and promiscuity in metalloenzymes Eom, Hyunuk; Song, Woon Ju JBIC Journal of Biological Inorganic Chemistry, Vol. 24, Issue 4 https://doi.org/10.1007/s00775-019-01667-0	journal	May 2019
Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals Maret, Wolfgang BioMetals, Vol. 22, Issue 1 https://doi.org/10.1007/s10534-008-9186-z	journal	January 2009
Soil factors associated with zinc deficiency in crops and humans Alloway, B. J. Environmental Geochemistry and Health, Vol. 31, Issue 5 https://doi.org/10.1007/s10653-009-9255-4	journal	March 2009
Photosynthetic rate, chlorophyll fluorescence parameters, and lipid peroxidation of maize leaves as affected by zinc deficiency Wang, H.; Jin, J. Y. Photosynthetica, Vol. 43, Issue 4 https://doi.org/10.1007/s11099-005-0092-0	journal	December 2005
Biofortification of major crop plants with iron and zinc - achievements and future directions Stangoulis, James C. R.; Knez, Marija Plant and Soil, Vol. 474, Issue 1-2 https://doi.org/10.1007/s11104-022-05330-7	journal	February 2022
Zng1 is a GTP-dependent zinc transferase needed for activation of methionine aminopeptidase Pasquini, Miriam; Grosjean, Nicolas; Hixson, Kim K. Cell Reports, Vol. 39, Issue 7 https://doi.org/10.1016/J.CELREP.2022.110834	journal	May 2022
Specificity for inhibitors of metal-substituted methionine aminopeptidase Li, Jing-Ya; Chen, Ling-Ling; Cui, Yong-Mei Biochemical and Biophysical Research Communications, Vol. 307, Issue 1 https://doi.org/10.1016/S0006-291X(03)01144-6	journal	July 2003
Alleviating hidden hunger: an infallible bridge to improved health and nutrition Das, Jai K.; Padhani, Zahra Ali The Lancet Global Health, Vol. 10, Issue 11 https://doi.org/10.1016/S2214-109X(22)00421-1	journal	November 2022
Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8 https://doi.org/10.1016/j.bbapap.2015.04.015	journal	August 2015
Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis Weiss, Andy; Murdoch, Caitlin C.; Edmonds, Katherine A. Cell, Vol. 185, Issue 12 https://doi.org/10.1016/j.cell.2022.04.011	journal	June 2022
LEFKOTHEA Regulates Nuclear and Chloroplast mRNA Splicing in Plants Daras, Gerasimos; Rigas, Stamatis; Alatzas, Anastasios Developmental Cell, Vol. 50, Issue 6 https://doi.org/10.1016/j.devcel.2019.07.024	journal	September 2019
Zinc in evolution Wiiliams, R. J. P. Journal of Inorganic Biochemistry, Vol. 111 https://doi.org/10.1016/j.jinorgbio.2012.01.004	journal	June 2012
Zinc coordination environments in proteins determine zinc functions Maret, Wolfgang Journal of Trace Elements in Medicine and Biology, Vol. 19, Issue 1 https://doi.org/10.1016/j.jtemb.2005.02.003	journal	September 2005
Decoding the Function of Expansion Segments in Ribosomes Fujii, Kotaro; Susanto, Teodorus Theo; Saurabh, Saumya Molecular Cell, Vol. 72, Issue 6 https://doi.org/10.1016/j.molcel.2018.11.023	journal	December 2018
Zinc Deficiency Limits the Photosynthetic Enzyme Activities in Zea mays K. Shrotri, C.; Mohanty, Prasanna; S. Rathore, V. Biochemie und Physiologie der Pflanzen, Vol. 178, Issue 2-3 https://doi.org/10.1016/s0015-3796(83)80034-1	journal	January 1983
Molecular cloning, sequencing, deletion, and overexpression of a methionine aminopeptidase gene from Saccharomyces cerevisiae. Chang, Y. H.; Teichert, U.; Smith, J. A. Journal of Biological Chemistry, Vol. 267, Issue 12 https://doi.org/10.1016/s0021-9258(18)42400-3	journal	April 1992
Tandem Mass Tags: A Novel Quantification Strategy for Comparative Analysis of Complex Protein Mixtures by MS/MS Thompson, Andrew; Schäfer, Jürgen; Kuhn, Karsten Analytical Chemistry, Vol. 75, Issue 8 https://doi.org/10.1021/ac0262560	journal	April 2003
Complex Chaperone Dependence of Rubisco Biogenesis Wilson, Robert H.; Hayer-Hartl, Manajit Biochemistry, Vol. 57, Issue 23 https://doi.org/10.1021/acs.biochem.8b00132	journal	March 2018
Physiologically Relevant Metal Cofactor for Methionine Aminopeptidase-2 Is Manganese Wang, Jieyi; Sheppard, George S.; Lou, Pingping Biochemistry, Vol. 42, Issue 17 https://doi.org/10.1021/bi020670c	journal	May 2003
Zinc through the Three Domains of Life Andreini, Claudia; Banci, Lucia; Bertini, Ivano Journal of Proteome Research, Vol. 5, Issue 11 https://doi.org/10.1021/pr0603699	journal	November 2006
Mass spectrometry-based proteomics Aebersold, Ruedi; Mann, Matthias Nature, Vol. 422, Issue 6928 https://doi.org/10.1038/nature01511	journal	March 2003
A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.) Rinke, Christian; Rubino, Francesco; Messer, Lauren F. The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0282-y	journal	October 2018
Calculating metalation in cells reveals CobW acquires CoII for vitamin B12 biosynthesis while related proteins prefer ZnII Young, Tessa R.; Martini, Maria Alessandra; Foster, Andrew W. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21479-8	journal	February 2021
Adaptive responses of marine diatoms to zinc scarcity and ecological implications Kellogg, Riss M.; Moosburner, Mark A.; Cohen, Natalie R. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29603-y	journal	April 2022
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Clustergrammer, a web-based heatmap visualization and analysis tool for high-dimensional biological data Fernandez, Nicolas F.; Gundersen, Gregory W.; Rahman, Adeeb Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.151	journal	October 2017
Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots Rodríguez-Celma, Jorge; Tsai, Yi-Hsiu; Wen, Tuan-Nan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35846	journal	November 2016
The labile zinc pool in plant cells Zlobin, Ilya E.; Kartashov, Alexander V.; Nosov, Alexander V. Functional Plant Biology, Vol. 46, Issue 9 https://doi.org/10.1071/FP19064	journal	January 2019
History of biological metal utilization inferred through phylogenomic analysis of protein structures Dupont, C. L.; Butcher, A.; Valas, R. E. Proceedings of the National Academy of Sciences, Vol. 107, Issue 23 https://doi.org/10.1073/pnas.0912491107	journal	May 2010
Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Li, X.; Chang, Y. H. Proceedings of the National Academy of Sciences, Vol. 92, Issue 26 https://doi.org/10.1073/pnas.92.26.12357	journal	December 1995
Zinc Deficiency Impacts CO ₂ Assimilation and Disrupts Copper Homeostasis in Chlamydomonas reinhardtii Malasarn, Davin; Kropat, Janette; Hsieh, Scott I. Journal of Biological Chemistry, Vol. 288, Issue 15 https://doi.org/10.1074/jbc.M113.455105	journal	February 2013
Metal Preferences and Metallation Foster, Andrew W.; Osman, Deenah; Robinson, Nigel J. Journal of Biological Chemistry, Vol. 289, Issue 41 https://doi.org/10.1074/jbc.R114.588145	journal	August 2014
N-terminal methionine excision of proteins creates tertiary destabilizing N-degrons of the Arg/N-end rule pathway Nguyen, Kha The; Kim, Jeong-Mok; Park, Sang-Eun Journal of Biological Chemistry, Vol. 294, Issue 12 https://doi.org/10.1074/jbc.RA118.006913	journal	January 2019
The Proteome of Copper, Iron, Zinc, and Manganese Micronutrient Deficiency in Chlamydomonas reinhardtii Hsieh, Scott I.; Castruita, Madeli; Malasarn, Davin Molecular & Cellular Proteomics, Vol. 12, Issue 1 https://doi.org/10.1074/mcp.M112.021840	journal	October 2012
Loss of blade photosynthetic area and of chloroplasts' photochemical capacity account for reduced CO2 assimilation rates in zinc-deficient sugar beet leaves Henriques, Fernando S. Journal of Plant Physiology, Vol. 158, Issue 7 https://doi.org/10.1078/0176-1617-00274	journal	January 2001
Generation of effective zinc-deficient agar-solidified media allows identification of root morphology changes in response to zinc limitation Sinclair, S. A.; Krämer, U. Plant Signaling & Behavior, Vol. 15, Issue 1 https://doi.org/10.1080/15592324.2019.1687175	journal	November 2019
Deciphering key features in protein structures with the new ENDscript server Robert, Xavier; Gouet, Patrice Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/NAR/GKU316	journal	April 2014
W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis Trifinopoulos, Jana; Nguyen, Lam-Tung; von Haeseler, Arndt Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/NAR/GKW256	journal	April 2016
BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks Maere, S.; Heymans, K.; Kuiper, M. Bioinformatics, Vol. 21, Issue 16 https://doi.org/10.1093/bioinformatics/bti551	journal	June 2005
COBALT: constraint-based alignment tool for multiple protein sequences Papadopoulos, J. S.; Agarwala, R. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm076	journal	March 2007
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Identification of eukaryotic peptide deformylases reveals universality of N-terminal protein processing mechanisms Giglione, C. The EMBO Journal, Vol. 19, Issue 21 https://doi.org/10.1093/emboj/19.21.5916	journal	November 2000
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
COG0523 proteins: a functionally diverse family of transition metal-regulated G3E P-loop GTP hydrolases from bacteria to man Edmonds, Katherine A.; Jordan, Matthew R.; Giedroc, David P. Metallomics, Vol. 13, Issue 8 https://doi.org/10.1093/mtomcs/mfab046	journal	July 2021
The role of nucleoside triphosphate hydrolase metallochaperones in making metalloenzymes Vaccaro, Francesca A.; Drennan, Catherine L. Metallomics, Vol. 14, Issue 6 https://doi.org/10.1093/mtomcs/mfac030	journal	April 2022
UniProt: the universal protein knowledgebase in 2021 Bateman, Alex; Martin, Maria-Jesus; Orchard, Sandra Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1100	journal	November 2020
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
Search and sequence analysis tools services from EMBL-EBI in 2022 Madeira, Fábio; Pearce, Matt; Tivey, Adrian R. N. Nucleic Acids Research, Vol. 50, Issue W1 https://doi.org/10.1093/nar/gkac240	journal	April 2022
Structural classification of zinc fingers: SURVEY AND SUMMARY Krishna, S. S. Nucleic Acids Research, Vol. 31, Issue 2 https://doi.org/10.1093/nar/gkg161	journal	January 2003
WoLF PSORT: protein localization predictor Horton, P.; Park, K. -J.; Obayashi, T. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm259	journal	May 2007
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
SUBA4: the interactive data analysis centre for Arabidopsis subcellular protein locations Hooper, Cornelia M.; Castleden, Ian R.; Tanz, Sandra K. Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1041	journal	November 2016
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update Tian, Tian; Liu, Yue; Yan, Hengyu Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx382	journal	May 2017
Functional Expression of Nitrile Hydratase in Escherichia coli: Requirement of a Nitrile Hydratase Activator and Post-Translational Modification of a Ligand Cysteine Nojiri, M.; Yohda, M.; Odaka, M. Journal of Biochemistry, Vol. 125, Issue 4 https://doi.org/10.1093/oxfordjournals.jbchem.a022339	journal	April 1999
Regulation of Root Nutrient Transporters by CIPK23: ‘One Kinase to Rule Them All’ Ródenas, Reyes; Vert, Grégory Plant and Cell Physiology, Vol. 62, Issue 4 https://doi.org/10.1093/pcp/pcaa156	journal	December 2020
Protein complex prediction with AlphaFold-Multimer Evans, Richard; O???Neill, Michael; Pritzel, Alexander https://doi.org/10.1101/2021.10.04.463034	preprint	March 2022
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Nucleoid-Enriched Proteomes in Developing Plastids and Chloroplasts from Maize Leaves: A New Conceptual Framework for Nucleoid Functions Majeran, Wojciech; Friso, Giulia; Asakura, Yukari Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/PP.111.188474	journal	November 2011
Functional and Developmental Impact of Cytosolic Protein N-Terminal Methionine Excision in Arabidopsis Ross, Simon; Giglione, Carmela; Pierre, Michèle Plant Physiology, Vol. 137, Issue 2 https://doi.org/10.1104/pp.104.056861	journal	February 2005
Identification of Three Urease Accessory Proteins That Are Required for Urease Activation in Arabidopsis Witte, Claus-Peter; Rosso, Mario G.; Romeis, Tina Plant Physiology, Vol. 139, Issue 3 https://doi.org/10.1104/pp.105.070292	journal	October 2005
Root Nutrient Foraging Giehl, R. F. H.; von Wiren, N. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.245225	journal	July 2014
Zinc Deficiency, Carbonic Anhydrase, and Photosynthesis in Leaves of Spinach Randall, P. J.; Bouma, D. Plant Physiology, Vol. 52, Issue 3 https://doi.org/10.1104/pp.52.3.229	journal	September 1973
pTAC2, -6, and -12 Are Components of the Transcriptionally Active Plastid Chromosome That Are Required for Plastid Gene Expression Pfalz, Jeannette; Liere, Karsten; Kandlbinder, Andrea The Plant Cell, Vol. 18, Issue 1 https://doi.org/10.1105/TPC.105.036392	journal	December 2005
Cotranslational Proteolysis Dominates Glutathione Homeostasis to Support Proper Growth and Development Frottin, Frédéric; Espagne, Christelle; Traverso, José A. The Plant Cell, Vol. 21, Issue 10 https://doi.org/10.1105/tpc.109.069757	journal	October 2009
A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus Xie, Meng; Muchero, Wellington; Bryan, Anthony C. The Plant Cell, Vol. 30, Issue 7 https://doi.org/10.1105/tpc.18.00168	journal	June 2018
Systemic Upregulation of MTP2- and HMA2-Mediated Zn Partitioning to the Shoot Supplements Local Zn Deficiency Responses Sinclair, Scott A.; Senger, Toralf; Talke, Ina N. The Plant Cell, Vol. 30, Issue 10 https://doi.org/10.1105/tpc.18.00207	journal	August 2018
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/GCE.2010.5676129	conference	November 2010
Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme: Reconstitution of the plastid RNA polymerase Suzuki, Jon Y.; Jimmy Ytterberg, A.; Beardslee, Thomas A. The Plant Journal, Vol. 40, Issue 1 https://doi.org/10.1111/J.1365-313X.2004.02195.X	journal	August 2004
Arabidopsis C‐terminal binding protein ANGUSTIFOLIA modulates transcriptional co‐regulation of MYB46 and WRKY33 Xie, Meng; Zhang, Jin; Yao, Tao New Phytologist, Vol. 228, Issue 5 https://doi.org/10.1111/NPH.16826	journal	August 2020
Carbonic anhydrases in plants and algae: Carbonic anhydrases in plants and algae Moroney, J. V.; Bartlett, S. G.; Samuelsson, G. Plant, Cell & Environment, Vol. 24, Issue 2 https://doi.org/10.1111/j.1365-3040.2001.00669.x	journal	February 2001
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Effect of Zinc Nutrition on Photosynthesis and Carbonic Anhydrase Activity in Cotton Ohki, K. Physiologia Plantarum, Vol. 38, Issue 4 https://doi.org/10.1111/j.1399-3054.1976.tb04007.x	journal	December 1976
Targeting of nucleus‐encoded proteins to chloroplasts in plants Jarvis, Paul New Phytologist, Vol. 179, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02452.x	journal	June 2008
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Bacillus subtilis FolE is sustained by the ZagA zinc metallochaperone and the alarmone ZTP under conditions of zinc deficiency Chandrangsu, Pete; Huang, Xiaojuan; Gaballa, Ahmed Molecular Microbiology, Vol. 112, Issue 3 https://doi.org/10.1111/mmi.14314	journal	June 2019
The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants Bang, Thomas Christian; Husted, Søren; Laursen, Kristian Holst New Phytologist, Vol. 229, Issue 5 https://doi.org/10.1111/nph.17074	journal	December 2020
Exploring the proteome associated with the mRNA encoding the D1 reaction center protein of Photosystem II in plant chloroplasts Watkins, Kenneth P.; Williams‐Carrier, Rosalind; Chotewutmontri, Prakitchai The Plant Journal, Vol. 102, Issue 2 https://doi.org/10.1111/tpj.14629	journal	January 2020
A Genomic Perspective on Protein Families Tatusov, R. L. Science, Vol. 278, Issue 5338 https://doi.org/10.1126/science.278.5338.631	journal	October 1997
Computed structures of core eukaryotic protein complexes Humphreys, Ian R.; Pei, Jimin; Baek, Minkyung Science, Vol. 374, Issue 6573 https://doi.org/10.1126/science.abm4805	journal	December 2021
Nucleotide sequence and genetic analysis of a 13.1-kilobase-pair Pseudomonas denitrificans DNA fragment containing five cob genes and identification of structural genes encoding Cob(I)alamin adenosyltransferase, cobyric acid synthase, and bifunctional cobinamide kinase-cobinamide phosphate guanylyltransferase Crouzet, J.; Levy-Schil, S.; Cameron, B. Journal of Bacteriology, Vol. 173, Issue 19 https://doi.org/10.1128/jb.173.19.6074-6087.1991	journal	October 1991
Zinc Competition among the Intestinal Microbiota Gielda, Lindsay M.; DiRita, Victor J. mBio, Vol. 3, Issue 4 https://doi.org/10.1128/mBio.00171-12	journal	July 2012
Zinc Proteins: Enzymes, Storage Proteins, Transcription Factors, and Replication Proteins Coleman, Joseph E. Annual Review of Biochemistry, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.bi.61.070192.004341	journal	June 1992
A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life Haas, Crysten E.; Rodionov, Dmitry A.; Kropat, Janette BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-470	journal	January 2009
Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells Lee, Lan-Ying; Fang, Mei-Jane; Kuang, Lin-Yun Plant Methods, Vol. 4, Issue 1 https://doi.org/10.1186/1746-4811-4-24	journal	January 2008
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Biofortification-A Sustainable Agricultural Strategy for Reducing Micronutrient Malnutrition in the Global South Bouis, Howarth E.; Welch, Ross M. Crop Science, Vol. 50 https://doi.org/10.2135/cropsci2009.09.0531	journal	March 2010
Redox regulation of the Calvin–Benson cycle: something old, something new Michelet, Laure; Zaffagnini, Mirko; Morisse, Samuel Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00470	journal	January 2013