Molecular Mechanisms Underlying Flax (Linum usitatissimum L.) Tolerance to Cadmium: A Case Study of Proteome and Metabolome of Four Different Flax Genotypes

. 2022 Oct 31 ; 11 (21) : . [epub] 20221031

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36365383

Grantová podpora
AF-IGA2021-IP053 Mendel University in Brno
MZE-RO1018 Ministry of Agriculture

Cadmium is one of the most toxic heavy metal pollutants, and its accumulation in the soil is harmful to agriculture. Plants have a higher cadmium tolerance than animals, and some species can be used for phytoremediation. Flax (Linum usitatissimum L.) can accumulate high amounts of cadmium, but the molecular mechanism behind its tolerance is unknown. Here, we employed four genotypes representing two fiber cultivars, an oilseed breeding line, and a transgenic line overexpressing the metallothionein domain for improved cadmium tolerance. We analyzed the proteome of suspensions and the proteome and metabolome of seedling roots in response to cadmium. We identified more than 1400 differentially abundant proteins representing putative mechanisms in cadmium tolerance, including metal-binding proteins and transporters, enzymes of flavonoid, jasmonate, polyamine, glutathione metabolism, and HSP70 proteins. Our data indicated the role of the phytohormone cytokinin in the observed responses. The metabolome profiling found that pipecolinic acid could be a part of the cadmium accumulation mechanism, and the observed accumulation of putrescine, coumaric acid, cinnamic acid, and coutaric acid confirmed the role of polyamines and flavonoids in tolerance to cadmium. In conclusion, our data provide new insight into cadmium tolerance and prospective targets for improving cadmium tolerance in other plants.

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Haider F.U., Liqun C., Coulter J.A., Cheema S.A., Wu J., Zhang R., Wenjun M., Farooq M. Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol. Environ. Saf. 2021;211:111887. doi: 10.1016/j.ecoenv.2020.111887. PubMed DOI

Hashem A., Abd_Allah E.F., Alqarawi A.A., Al Huqail A.A., Egamberdieva D., Wirth S. Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J. Biol. Sci. 2016;23:272–281. doi: 10.1016/j.sjbs.2015.11.002. PubMed DOI PMC

Khan S., Cao Q., Zheng Y.M., Huang Y.Z., Zhu Y.G. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 2008;152:686–692. doi: 10.1016/j.envpol.2007.06.056. PubMed DOI

Zhang M.-K., Liu Z.-Y., Wang H. Use of Single Extraction Methods to Predict Bioavailability of Heavy Metals in Polluted Soils to Rice. Commun. Soil Sci. Plant Anal. 2010;41:820–831. doi: 10.1080/00103621003592341. DOI

Salt D.E., Prince R.C., Pickering I.J., Raskin I. Mechanisms of Cadmium Mobility and Accumulation in Indian Mustard. Plant Physiol. 1995;109:1427–1433. doi: 10.1104/pp.109.4.1427. PubMed DOI PMC

Gallego S.M., Pena L.B., Barcia R.A., Azpilicueta C.E., Iannone M.F., Rosales E.P., Zawoznik M.S., Groppa M.D., Benavides M.P. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ. Exp. Bot. 2012;83:33–46. doi: 10.1016/j.envexpbot.2012.04.006. DOI

Schaefer H.R., Dennis S., Fitzpatrick S. Cadmium: Mitigation strategies to reduce dietary exposure. J. Food Sci. 2020;85:260–267. doi: 10.1111/1750-3841.14997. PubMed DOI PMC

Nazar R., Iqbal N., Masood A., Khan M.I.R., Syeed S., Khan N.A. Cadmium Toxicity in Plants and Role of Mineral Nutrients in Its Alleviation. Am. J. Plant Sci. 2012;3:1476–1489. doi: 10.4236/ajps.2012.310178. DOI

Ismael M.A., Elyamine A.M., Moussa M.G., Cai M., Zhao X., Hu C. Cadmium in plants: Uptake, toxicity, and its interactions with selenium fertilizers. Metallomics. 2019;11:255–277. doi: 10.1039/C8MT00247A. PubMed DOI

Genchi G., Sinicropi M.S., Lauria G., Carocci A., Catalano A. The Effects of Cadmium Toxicity. Int. J. Environ. Res. Public Health. 2020;17:3782. doi: 10.3390/ijerph17113782. PubMed DOI PMC

Abbas T., Rizwan M., Ali S., Adrees M., Zia-ur-Rehman M., Qayyum M.F., Ok Y.S., Murtaza G. Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ. Sci. Pollut. Res. 2018;25:25668–25680. doi: 10.1007/s11356-017-8987-4. PubMed DOI

Gratão P.L., Monteiro C.C., Rossi M.L., Martinelli A.P., Peres L.E.P., Medici L.O., Lea P.J., Azevedo R.A. Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ. Exp. Bot. 2009;67:387–394. doi: 10.1016/j.envexpbot.2009.06.017. DOI

Xue Z.-C., Gao H.-Y., Zhang L.-T. Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol. Plant. 2013;57:587–590. doi: 10.1007/s10535-013-0318-0. DOI

Jhala A.J., Hall L.M. Flax (Linum usitatissimum L.): Current uses and future applications. Aust. J. Basic Appl. Sci. 2010;4:4304–4312.

Fucassi F., Heikal A., Mikhalovska L.I., Standen G., Allan I.U., Mikhalovsky S.V., Cragg P.J. Metal chelation by a plant lignan, secoisolariciresinol diglucoside. J. Incl. Phenom. Macrocycl. Chem. 2014;80:345–351. doi: 10.1007/s10847-014-0411-9. DOI

Angelova V., Ivanova R., Delibaltova V., Ivanov K. Bio-accumulation and distribution of heavy metals in fibre crops (flax, cotton and hemp) Ind. Crops Prod. 2004;19:197–205. doi: 10.1016/j.indcrop.2003.10.001. DOI

Smykalova I., Vrbova M., Tejklova E., Vetrovcova M., Griga M. Large scale screening of heavy metal tolerance in flax/linseed (Linum usitatissimum L.) tested in vitro. Ind. Crops Prod. 2010;32:527–533. doi: 10.1016/j.indcrop.2010.06.027. DOI

Bjelková M., Genčurová V., Griga M. Accumulation of cadmium by flax and linseed cultivars in field-simulated conditions: A potential for phytoremediation of Cd-contaminated soils. Ind. Crops Prod. 2011;33:761–774. doi: 10.1016/j.indcrop.2011.01.020. DOI

Ueno D., Milner M.J., Yamaji N., Yokosho K., Koyama E., Clemencia Zambrano M., Kaskie M., Ebbs S., Kochian L.V., Ma J.F. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J. 2011;66:852–862. doi: 10.1111/j.1365-313X.2011.04548.x. PubMed DOI

Hradilová J., Řehulka P., Řehulková H., Vrbová M., Griga M., Brzobohatý B. Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis. 2010;31:421–431. doi: 10.1002/elps.200900477. PubMed DOI

Höckner M., Piechnik C.A., Fiechtner B., Weinberger B., Tomanek L. Cadmium-Related Effects on Cellular Immunity Comprises Altered Metabolism in Earthworm Coelomocytes. Int. J. Mol. Sci. 2020;21:599. doi: 10.3390/ijms21020599. PubMed DOI PMC

Daniel B., Wallner S., Steiner B., Oberdorfer G., Kumar P., van der Graaff E., Roitsch T., Sensen C.W., Gruber K., Macheroux P. Structure of a Berberine Bridge Enzyme-Like Enzyme with an Active Site Specific to the Plant Family Brassicaceae. PLoS ONE. 2016;11:e0156892. doi: 10.1371/journal.pone.0156892. PubMed DOI PMC

Hyun T.K., van der Graaff E., Albacete A., Eom S.H., Großkinsky D.K., Böhm H., Janschek U., Rim Y., Ali W.W., Kim S.Y., et al. The Arabidopsis PLAT Domain Protein1 Is Critically Involved in Abiotic Stress Tolerance. PLoS ONE. 2014;9:e112946. doi: 10.1371/journal.pone.0112946. PubMed DOI PMC

Krapivinsky G.B., Ackerman M.J., Gordon E.A., Krapivinsky L.D., Clapham D.E. Molecular characterization of a swelling-induced chloride conductance regulatory protein, plCIn. Cell. 1994;76:439–448. doi: 10.1016/0092-8674(94)90109-0. PubMed DOI

Collings D.A., Gebbie L.K., Howles P.A., Hurley U.A., Birch R.J., Cork A.H., Hocart C.H., Arioli T., Williamson R.E. Arabidopsis dynamin-like protein DRP1A: A null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion. J. Exp. Bot. 2008;59:361–376. doi: 10.1093/jxb/erm324. PubMed DOI

Gutierrez-Beltran E., Moschou P.N., Smertenko A.P., Bozhkov P.V. Tudor Staphylococcal Nuclease Links Formation of Stress Granules and Processing Bodies with mRNA Catabolism in Arabidopsis. Plant Cell. 2015;27:926–943. doi: 10.1105/tpc.114.134494. PubMed DOI PMC

Dutilleul C., Jourdain A., Bourguignon J., Hugouvieux V. The Arabidopsis Putative Selenium-Binding Protein Family: Expression Study and Characterization of SBP1 as a Potential New Player in Cadmium Detoxification Processes. Plant Physiol. 2008;147:239–251. doi: 10.1104/pp.107.114033. PubMed DOI PMC

Amaral dos Reis R., Hendrix S., Mourato M.P., Louro Martins L., Vangronsveld J., Cuypers A. Efficient regulation of copper homeostasis underlies accession-specific sensitivities to excess copper and cadmium in roots of Arabidopsis thaliana. J. Plant Physiol. 2021;261:153434. doi: 10.1016/j.jplph.2021.153434. PubMed DOI

Heo D.-H., Baek I.-J., Kang H.-J., Kim J.-H., Chang M., Jeong M.-Y., Kim T.-H., Choi I.-D., Yun C.-W. Cadmium regulates copper homoeostasis by inhibiting the activity of Mac1, a transcriptional activator of the copper regulon, in Saccharomyces cerevisiae. Biochem. J. 2010;431:257–265. doi: 10.1042/BJ20100638. PubMed DOI

Griga M., Bjelkova M., Tejklová E. Potential of flax (Linum usitatissimum L.) for heavy metal phytoextraction and industrial processing of contaminated biomass—A review. In: Mench M., Mocquot B., editors. Risk Assessment and Sustainable Land Management Using Plants in Trace Elements-Contaminated Soils. Institut National de la Recherche Agronomique; Villenave d’Ornon, France: 2003. pp. 173–179.

Soudek P., Katrušáková A., Sedláček L., Petrová Š., Kočí V., Maršík P., Griga M., Vaněk T. Effect of Heavy Metals on Inhibition of Root Elongation in 23 Cultivars of Flax (Linum usitatissimum L.) Arch. Environ. Contam. Toxicol. 2010;59:194–203. doi: 10.1007/s00244-010-9480-y. PubMed DOI

Son J.-H., Park K.-C., Lee S.-I., Kim H.-H., Kim J.-H., Kim S.-H., Kim N.-S. Isolation of cold-responsive genes from garlic, Allium sativum. Genes Genom. 2012;34:93–101. doi: 10.1007/s13258-011-0187-x. DOI

Bernsdorff F., Döring A.-C., Gruner K., Schuck S., Bräutigam A., Zeier J. Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways. Plant Cell. 2016;28:102–129. doi: 10.1105/tpc.15.00496. PubMed DOI PMC

Seifikalhor M., Aliniaeifard S., Bernard F., Seif M., Latifi M., Hassani B., Didaran F., Bosacchi M., Rezadoost H., Li T. γ-Aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Sci. Rep. 2020;10:3356. doi: 10.1038/s41598-020-59592-1. PubMed DOI PMC

Groppa M.D., Tomaro M.L., Benavides M.P. Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci. 2001;161:481–488. doi: 10.1016/S0168-9452(01)00432-0. DOI

Groppa M.D., Tomaro M.L., Benavides M.P. Polyamines and heavy metal stress: The antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. BioMetals. 2007;20:185–195. doi: 10.1007/s10534-006-9026-y. PubMed DOI

Hsu Y.T., Kao C.H. Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil. 2007;291:27–37. doi: 10.1007/s11104-006-9171-7. DOI

Lei G.J., Sun L., Sun Y., Zhu X.F., Li G.X., Zheng S.J. Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. J. Integr. Plant Biol. 2020;62:218–227. doi: 10.1111/jipb.12801. PubMed DOI

Černý M., Novák J., Habánová H., Cerna H., Brzobohatý B. Role of the proteome in phytohormonal signaling. Biochim. Biophys. Acta-Proteins Proteom. 2016;1864:1003–1015. doi: 10.1016/j.bbapap.2015.12.008. PubMed DOI

Lu Q., Chen S., Li Y., Zheng F., He B., Gu M. Exogenous abscisic acid (ABA) promotes cadmium (Cd) accumulation in Sedum alfredii Hance by regulating the expression of Cd stress response genes. Environ. Sci. Pollut. Res. 2020;27:8719–8731. doi: 10.1007/s11356-019-07512-w. PubMed DOI

Chen K., Chen P., Qiu X., Chen J., Gao G., Wang X., Zhu A., Yu C. Regulating role of abscisic acid on cadmium enrichment in ramie (Boehmeria nivea L.) Sci. Rep. 2021;11:22045. doi: 10.1038/s41598-021-00322-6. PubMed DOI PMC

Pavlů J., Novák J., Koukalová V., Luklová M., Brzobohatý B., Černý M. Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways. Int. J. Mol. Sci. 2018;19:2450. doi: 10.3390/ijms19082450. PubMed DOI PMC

Brenner W.G., Schmülling T. Transcript profiling of cytokinin action in Arabidopsis roots and shoots discovers largely similar but also organ-specific responses. BMC Plant Biol. 2012;12:112. doi: 10.1186/1471-2229-12-112. PubMed DOI PMC

Pavlů J., Kerchev P., Černý M., Novák J., Berka M., Jobe T.O., López-Ramos J.M., Saiz-Fernández I., Rashotte A.M., Kopriva S., et al. Cytokinin modulates sulfur and glutathione metabolic network. J. Exp. Bot. 2022 doi: 10.1093/jxb/erac391. in print. PubMed DOI

Berka M., Kopecká R., Berková V., Brzobohatý B., Černý M. Regulation of heat shock proteins 70 and their role in plant immunity. J. Exp. Bot. 2022;73:1894–1909. doi: 10.1093/jxb/erab549. PubMed DOI PMC

Sriram M., Osipiuk J., Freeman B.C., Morimoto R.I., Joachimiak A. Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure. 1997;5:403–414. doi: 10.1016/S0969-2126(97)00197-4. PubMed DOI

Begum N., Hu Z., Cai Q., Lou L. Influence of PGPB Inoculation on HSP70 and HMA3 Gene Expression in Switchgrass under Cadmium Stress. Plants. 2019;8:504. doi: 10.3390/plants8110504. PubMed DOI PMC

Li X., Zheng H., Shi L., Liu Z., He L., Gao J. Stress-seventy subfamily A 4, A member of HSP70, confers yeast cadmium tolerance in the loss of mitochondria pyruvate carrier 1. Plant Signal. Behav. 2020;15:1719312. doi: 10.1080/15592324.2020.1719312. PubMed DOI PMC

Guan C., Jin C., Ji J., Wang G., Li X. LcBiP, a endoplasmic reticulum chaperone binding protein gene from Lycium chinense, confers cadmium tolerance in transgenic tobacco. Biotechnol. Prog. 2015;31:358–368. doi: 10.1002/btpr.2046. PubMed DOI

Wang T., Yuan Y., Zou H., Yang J., Zhao S., Ma Y., Wang Y., Bian J., Liu X., Gu J., et al. The ER stress regulator Bip mediates cadmium-induced autophagy and neuronal senescence. Sci. Rep. 2016;6:38091. doi: 10.1038/srep38091. PubMed DOI PMC

De Benedictis M., Gallo A., Migoni D., Papadia P., Roversi P., Santino A. Cadmium treatment induces endoplasmic reticulum stress and unfolded protein response in Arabidopsis thaliana. bioRxiv. 2022 doi: 10.1101/2022.09.23.509148. PubMed DOI

Yuan B., Yang Y., Fan P., Liu J., Xing H., Liu Y., Feng D. Genome-Wide Identification and Characterization of Germin and Germin-Like Proteins (GLPs) and Their Response Under Powdery Mildew Stress in Wheat (Triticum aestivum L.) Plant Mol. Biol. Report. 2021;39:821–832. doi: 10.1007/s11105-021-01291-w. DOI

Zhang Y., Wang X., Chang X., Sun M., Zhang Y., Li W., Li Y. Overexpression of germin-like protein GmGLP10 enhances resistance to Sclerotinia sclerotiorum in transgenic tobacco. Biochem. Biophys. Res. Commun. 2018;497:160–166. doi: 10.1016/j.bbrc.2018.02.046. PubMed DOI

Pei Y., Li X., Zhu Y., Ge X., Sun Y., Liu N., Jia Y., Li F., Hou Y. GhABP19, a Novel Germin-Like Protein From Gossypium hirsutum, Plays an Important Role in the Regulation of Resistance to Verticillium and Fusarium Wilt Pathogens. Front. Plant Sci. 2019;10:583. doi: 10.3389/fpls.2019.00583. PubMed DOI PMC

Cerny M., Berka M., Dvořák M., Milenković I., Saiz-Fernández I., Brzobohatý B., Ďurkovič J. Defense mechanisms promoting tolerance to aggressive Phytophthora species in hybrid poplar. Front. Plant Sci. 2022;13:1018272. doi: 10.3389/fpls.2022.1018272. PubMed DOI PMC

Farooq M.A., Niazi A.K., Akhtar J., Saifullah, Farooq M., Souri Z., Karimi N., Rengel Z. Acquiring control: The evolution of ROS-Induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol. Biochem. 2019;141:353–369. doi: 10.1016/j.plaphy.2019.04.039. PubMed DOI

Wu Z., Liu S., Zhao J., Wang F., Du Y., Zou S., Li H., Wen D., Huang Y. Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ. Exp. Bot. 2017;133:1–11. doi: 10.1016/j.envexpbot.2016.09.005. DOI

Qin S., Liu H., Nie Z., Gao W., Li C., Lin Y., Zhao P. AsA–GSH Cycle and Antioxidant Enzymes Play Important Roles in Cd Tolerance of Wheat. Bull. Environ. Contam. Toxicol. 2018;101:684–690. doi: 10.1007/s00128-018-2471-9. PubMed DOI

Chen S., Lin R., Lu H., Wang Q., Yang J., Liu J., Yan C. Effects of phenolic acids on free radical scavenging and heavy metal bioavailability in Kandelia obovata under cadmium and zinc stress. Chemosphere. 2020;249:126341. doi: 10.1016/j.chemosphere.2020.126341. PubMed DOI

Vrbová M., Kotrba P., Horáček J., Smýkal P., Švábová L., Větrovcová M., Smýkalová I., Griga M. Enhanced accumulation of cadmium in Linum usitatissimum L. plants due to overproduction of metallothionein α-domain as a fusion to β-glucuronidase protein. Plant Cell Tissue Organ Cult. 2013;112:321–330. doi: 10.1007/s11240-012-0239-1. DOI

Cvečková M., Smýkalová I., Větrovcová M., Vrbová M. Testing of Heavy Metals Toxicity with Suspension Cultures of Hemp (Cannabis sativa ssp. sativa L.) Agritec; Šumperk, Czech Republic: 2015.

Yaru B., Bainok D., Day G. Determination of Cd, Cu, Pb, and Zn in biological tissues using Zeeman graphite furnace AAS after microwave digestion in non-pressurized, semi-closed vessel. At. Spectrosc. 1999;20:33–38.

Berka M., Greplová M., Saiz-Fernández I., Novák J., Luklová M., Zelená P., Tomšovský M., Brzobohatý B., Černý M. Peptide-based identification of Phytophthora isolates and Phytophthora detection in planta. Int. J. Mol. Sci. 2020;21:9463. doi: 10.3390/ijms21249463. PubMed DOI PMC

Saiz-Fernández I., Milenković I., Berka M., Černý M., Tomšovský M., Brzobohatý B., Kerchev P. Integrated Proteomic and Metabolomic Profiling of Phytophthora cinnamomi Attack on Sweet Chestnut (Castanea sativa) Reveals Distinct Molecular Reprogramming Proximal to the Infection Site and Away from It. Int. J. Mol. Sci. 2020;21:8525. doi: 10.3390/ijms21228525. PubMed DOI PMC

Dufková H., Berka M., Greplová M., Shejbalová Š., Hampejsová R., Luklová M., Domkářová J., Novák J., Kopačka V., Brzobohatý B., et al. The Omics Hunt for Novel Molecular Markers of Resistance to Phytophthora infestans. Plants. 2022;11:61. doi: 10.3390/plants11010061. PubMed DOI PMC

Wang Z., Hobson N., Galindo L., Zhu S., Shi D., McDill J., Yang L., Hawkins S., Neutelings G., Datla R., et al. The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J. 2012;72:461–473. doi: 10.1111/j.1365-313X.2012.05093.x. PubMed DOI

Szklarczyk D., Gable A.L., Lyon D., Junge A., Wyder S., Huerta-Cepas J., Simonovic M., Doncheva N.T., Morris J.H., Bork P., et al. STRING v11: Protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607–D613. doi: 10.1093/nar/gky1131. PubMed DOI PMC

Berka M., Luklová M., Dufková H., Berková V., Novák J., Saiz-Fernández I., Rashotte A.M., Brzobohaty B., Cerny M. Barley root proteome and metabolome in response to cytokinin and abiotic stimuli. Front. Plant Sci. 2020;11:590337. doi: 10.3389/fpls.2020.590337. PubMed DOI PMC

Hampejsová R., Berka M., Berková V., Jersáková J., Domkářová J., von Rundstedt F., Frary A., Saiz-Fernández I., Brzobohatý B., Černý M. Interaction with Fungi Promotes the Accumulation of Specific Defense Molecules in Orchid Tubers and May Increase the Value of Tubers for Biotechnological and Medicinal Applications: The Case Study of Interaction Between Dactylorhiza sp. and Tulasnella calospora. Front. Plant Sci. 2022;13:757852. doi: 10.3389/fpls.2022.757852. PubMed DOI PMC

Pino L.K., Searle B.C., Bollinger J.G., Nunn B., MacLean B., MacCoss M.J. The Skyline ecosystem: Informatics for quantitative mass spectrometry proteomics. Mass Spectrom. Rev. 2020;39:229–244. doi: 10.1002/mas.21540. PubMed DOI PMC

Pang Z., Chong J., Zhou G., De Lima Morais D.A., Chang L., Barrette M., Gauthier C., Jacques P.É., Li S., Xia J. MetaboAnalyst 5.0: Narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021;49:W388–W396. doi: 10.1093/nar/gkab382. PubMed DOI PMC

Zhou G., Ewald J., Xia J. OmicsAnalyst: A comprehensive web-based platform for visual analytics of multi-omics data. Nucleic Acids Res. 2021;49:W476–W482. doi: 10.1093/nar/gkab394. PubMed DOI PMC

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