[en] During evolution, plants have faced countless stresses of both biotic and abiotic nature developing very effective mechanisms able to perceive and counteract adverse signals. The biggest challenge is the ability to fine-tune the trade-off between plant growth and stress resistance. The Antarctic plant Colobanthus quitensis has managed to survive the adverse environmental conditions of the white continent and can be considered a wonderful example of adaptation to prohibitive conditions for millions of other plant species. Due to the progressive environmental change that the Antarctic Peninsula has undergone over time, a more comprehensive overview of the metabolic features of C. quitensis becomes particularly interesting to assess its ability to respond to environmental stresses. To this end, a differential proteomic approach was used to study the response of C. quitensis to different environmental cues. Many differentially expressed proteins were identified highlighting the rewiring of metabolic pathways as well as defense responses. Finally, a different modulation of oxidative stress response between different environmental sites was observed. The data collected in this paper add knowledge on the impact of environmental stimuli on plant metabolism and stress response by providing useful information on the trade-off between plant growth and defense mechanisms.
Bertini, Laura; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Proietti, Silvia ; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Fongaro, Benedetta ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS) ; Department of Pharmaceutical and Pharmacological Sciences, University of Padova, 35100 Padova, Italy
Holfeld, Aleš; Institute of Molecular Systems Biology, Department of Biology, ETH Zurich, 8093 Zurich, Switzerland
Picotti, Paola; Institute of Molecular Systems Biology, Department of Biology, ETH Zurich, 8093 Zurich, Switzerland
Falconieri, Gaia Salvatore ; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Bizzarri, Elisabetta; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Capaldi, Gloria; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Polverino de Laureto, Patrizia ; Department of Pharmaceutical and Pharmacological Sciences, University of Padova, 35100 Padova, Italy
Caruso, Carla ; Department of Ecological and Biological Sciences, University of Tuscia, 01100 Viterbo, Italy
Language :
English
Title :
Environmental Signals Act as a Driving Force for Metabolic and Defense Responses in the Antarctic Plant Colobanthus quitensis.
MIUR - Ministry of Education, University and Research [IT]
Funding text :
This research was funded by Ministry of University and Scientific Research (MUR), in the framework of the PNRA (National Program for Antarctic Research), grant number PNRA16_00068.The authors wish to thank the INACH (Instituto Antártico Chileno) for the logistic support from Chile to King George Island and vice versa and the Henrik Arctowski Research Station members for their great hospitality and collaboration with logistics. We also thank our colleague Cristina Moscatelli for the soil texture analyses. This paper is dedicated to the beloved memory of our colleague and friend Marina Tucci.
Convey P. Coulson S.J. Worland M.R. Sjöblom A. The importance of understanding annual and shorter-term temperature patterns and variation in the surface levels of polar soils for terrestrial biota Polar. Biol. 2018 41 1587 1605 10.1007/s00300-018-2299-0
Sierra-Almeida A. Cavieres L.A. Bravo L.A. Warmer temperatures affect the in situ freezing resistance of the Antarctic vascular plants Front. Plant. Sci. 2018 9 1456 10.3389/fpls.2018.01456 30349551
Clemente-Moreno M.J. Omranian N. Sáez P. Figureueroa C.M. Del-Saez N. Elso M. Poblete L. Orf I. Cuadros-Inostroza A. Cavieres L. et al. Cytochrome respiration pathway and sulphur metabolism sustain stress tolerance to low temperature in the Antarctic species Colobanthus quitensis New Phytol. 2020 225 754 768 10.1111/nph.16167 31489634
Alberdi M. Bravo L.A. Gutiérrez A. Gidekel M. Corcuera L.J. Ecophysiology of Antarctic vascular plants Physiol. Plantarum. 2002 115 479 486 10.1034/j.1399-3054.2002.1150401.x 12121453
Wasley J. Robinson S.A. Lovelock C.E. Popp M. Climate change manipulations show Antarctic flora is more strongly affected by elevated nutrients than water Global. Change Biol. 2006 12 1800 1812 10.1111/j.1365-2486.2006.01209.x
Convey P. Antarctic terrestrial biodiversity in a changing world Polar Biol. 2011 34 1629 1641 10.1007/s00300-011-1068-0
Robinson S.A. King D.H. Bramley-Alves J. Waterman M.J. Ashcroft M.B. Wasley J. Turnbull J.D. Miller R.E. Ryan-Colton E. Benny T. et al. Rapid change in East Antarctic terrestrial vegetation in response to regional drying Nat. Clim. Change 2018 8 879 884 10.1038/s41558-018-0280-0
Cavieres L.A. Sáez P. Sanhueza C. Sierra-Almeida A. Rabert C. Corcuera L.J. Alberdi M. Bravo L.A. Ecophysiological traits of Antarctic vascular plants: Their importance in the responses to climate change Plant Ecol. 2016 217 343 358 10.1007/s11258-016-0585-x
Pertierra L.R. Lara F. Benayas J. Hughes K.A. Poa pratensis L., current status of the longest-established non-native vascular plant in the Antarctic Polar Biol. 2013 36 1473 1481 10.1007/s00300-013-1367-8
Chwedorzewska K.J. Giełwanowska I. Olech M. Molina-Montenegro M.A. Wódkiewicz M. Galera H. Poa annua L. in the maritime Antarctic: An overview Polar Rec. 2015 51 637 643 10.1017/S0032247414000916
Cuba-Díaz M. Troncoso J. Cordero C. Finot V. Rondanelli-Reyes M. Juncus bufonius, a new non-native vascular plant in King George Island, South Shetland Islands Antarct. Sci. 2013 25 385 386 10.1017/S0954102012000958
Convey P. Hopkins D. Roberts S. Tyler A. Global southern limit of flowering plants and moss peat accumulation Polar Res. 2011 30 8929 10.3402/polar.v30i0.8929
Smith R.I.L. The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica Antarctic Biology in a Global Context Huiskes A.H.L. Gieskes W.W.C. Rozema J. Schorno R.M.L. van der Vies S.M. Wolff W.J. Backhuys Leiden, The Netherlands 2003 234 239
Reyes-Bahamonde C. Consecuencias del aumento de la temperatura y la sequía en la Resistencia al Congelamiento de Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth.) Bartl. (Caryophyllaceae) Undergraduate Thesis Universidad de Concepción Concepción, Chile 2013
Giełwanowska I. Pastorczyk M. Kellmann-Sopyła W. Gorniak D. Gorecki R.J. Morphological and ultrastructural changes of organelles in leaf mesophyll cells of the Arctic and Antarctic plants of Poaceae family under cold influence Arct. Antarct. Alp. Res. 2015 47 17 25 10.1657/AAAR0014-019
Acuña-Rodríguez I.S. Torres-Díaz C. Hereme R. Molina-Montenegro M.A. Asymmetric responses to simulated global warming by populations of Colobanthus quitensis along a latitudinal gradient PeerJ 2017 5 e3718 10.7717/peerj.3718 28948096
Cannone N. Guglielmin M. Convey P. Worland M.R. Favero Longo S.E. Vascular plant changes in extreme environments: Effects of multiple drivers Clim. Change 2016 134 651 665 10.1007/s10584-015-1551-7
Cannone N. Malfasi F. Favero-Longo S.E. Convey P. Guglielmin M. Acceleration of climate warming and plant dynamics in Antarctica Curr. Biol. 2022 32 1599 1606 10.1016/j.cub.2022.01.074 35167803
Hereme R. Morales-Navarro S. Ballesteros G. Barrera A. Ramos P. Gundel P.E. Molina-Montenegro M.A. Fungal endophytes exert positive effects on Colobanthus quitensis under water stress but neutral under a projected climate change scenario in Antarctica Front Microbiol. 2020 11 264 10.3389/fmicb.2020.00264 32184767
Torres-Díaz C. Gallardo-Cerda J. Lavin P. Oses R. Carrasco-Urra F. Atala C. Acuña-Rodríguez I.S. Convey P. Molina-Montenegro M.A. Biological interactions and simulated climate change modulates the ecophysiological performance of Colobanthus quitensis in the Antarctic ecosystem PLoS ONE 2016 11 e0164844 10.1371/journal.pone.0164844
Bertini L. Perazzolli M. Proietti S. Capaldi G. Savatin D.V. Bigini V. Longa C.M.O. Basaglia M. Favaro L. Casella S. et al. Biodiversity and Bioprospecting of Fungal Endophytes from the Antarctic Plant Colobanthus quitensis J. Fungi 2022 8 979 10.3390/jof8090979
Arthofer W. Bertini L. Caruso C. Cicconardi F. Delph L.F. Fields P.D. Ikeda M. Minegishi Y. Proietti S. Ritthammer H. et al. Transcriptome sequencing of the Antarctic Colobanthus quitensis (Kunth) Bartl (Caryophillaceae) Mol. Ecol. Resour. 2015 15 1014 1015 10.1111/1755-0998.12419
Bertini L. Cozzolino F. Proietti S. Falconieri G.S. Iacobucci I. Salvia R. Falabella P. Monti M. Caruso C. What Antarctic plants can tell us about climate changes: Temperature as a driver for metabolic reprogramming Biomolecules 2021 11 1094 10.3390/biom11081094 34439761
Cho S.M. Lee H. Jo H. Lee H. Kang Y. Park H. Lee J. Comparative transcriptome analysis of field- and chamber-grown samples of Colobanthus quitensis (Kunth) Bartl, an Antarctic flowering plant Sci. Rep. 2018 8 11049 10.1038/s41598-018-29335-4 30038328
Bertini L. Palazzi L. Proietti S. Pollastri S. Arrigoni G. Polverino de Laureto P. Caruso C. Proteomic analysis of MeJa-induced defense responses in rice against wounding Int. J. Mol. Sci. 2019 20 2525 10.3390/ijms20102525 31121967
Ge S.X. Jung D. Yao R. ShinyGO: A graphical gene-set enrichment tool for animals and plants Bioinformatics 2020 36 2628 2629 10.1093/bioinformatics/btz931 31882993
Samyshev E.Z. Minkina N.I. Coastal Ecosystem Contamination by Heavy Metals as an Indicator of Climate Change in Antarctica J. Comput. Theor. Nanosci. 2019 16 1 10.1166/jctn.2019.7729
Hughes K.A. Threats to soil communities: Human impacts Antarctic Terrestrial Microbiology: Physical and Biological Properties of Antarctic Soils Cowan D.A. Springer Berlin/Heidelberg, Germany 2014 263 277 10.1007/978-3-642-45213-0_14
Chmielowska-Bąk J. Gzyl J. Ruścińska-Sobkowiak R. Arasimowicz-Jelonek M. Deckert J. The new insights into cadmium sensing Front Plant Sci. 2014 5 245 10.3389/fpls.2014.00245
Dorta D.J. Leite S. Demarco K.C. Prado I.M. Rodrigues T. Mingatto F.E. Uyemura S.A. Santos A.C. Curti C. A proposed sequence of events for cadmium-induced mitochondrial impairment J. Inorg. Biochem. 2003 97 251 257 10.1016/S0162-0134(03)00314-3
Pastuszak J. Kopeć P. Płażek A. Gondek K. Szczerba A. Hornyák M. Dubert F. Antioxidant activity as a response to cadmium pollution; in three durum wheat genotypes differing in salt-tolerance Open Chem. 2020 18 1230 1241 10.1515/chem-2020-0113
Ohi R. Feoktistova A. McCann S. Virginia Valentine V. Look A.T. Lipsick J.S. Gould L.K. Myb-related Schizosaccharomyces pombe cdc5p is structurally and functionally conserved in eukaryotes Mol. Cell. Biol. 1998 18 4097 4108 10.1128/MCB.18.7.4097
Hirayama T. Shinozaki K. A cdc5+ homolog of a higher plant, Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 1996 93 13371 13376 10.1073/pnas.93.23.13371
Burns C.G. Ohi R. Krainer A.R. Gould K.L. Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing Proc. Natl. Acad. Sci. USA 1999 96 13789 13794 10.1073/pnas.96.24.13789 10570151
McDonald W.H. Ohi R. Smelkova N. Frendewey D. Gould K.L. Myb-related fission yeast CDC5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing Mol. Cell. Biol. 1999 19 5352 5362 10.1128/MCB.19.8.5352 10409726
Palma K. Zhao Q. Cheng Y.T. Bi D. Monaghan J. Cheng W. Zhang Y. Li X. Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms Genes Dev. 2007 21 1484 1493 10.1101/gad.1559607 17575050
Lin Z. Yin Z. Zhu D. Chen Z. Gu H. Qu L.J. AtCDC5 regulates the G2 to M transition of the cell cycle and is critical for the function of Arabidopsis shoot apical meristem Cell Res. 2007 17 815 828 10.1038/cr.2007.71
Ikram Z. Mouna G. Faiçal B. Pathogenesis Related Proteins (PRs): From Cellular Mechanisms to Plant Defense Curr. Protein Pept. Sci. 2021 22 396 412 10.2174/1389203721999201231212736
Bertini L. Leonardi L. Caporale C. Tucci M. Cascone A. Di Berardino I. Buonocore V. Caruso C. Pathogen-responsive wheat PR4 genes are induced by activators of systemic acquired resistance and wounding Plant Sci. 2003 164 1067 1078 10.1016/S0168-9452(03)00112-2
De Lorenzo G. D’Ovidio R. Felice Cervone F. The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi Annu. Rev. Phytopathol. 2001 39 313 335 10.1146/annurev.phyto.39.1.313
Cecchini N. Steffes K. Schläppi M.R. Gifford A.N. Greenberg J.T. Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming Nat. Commun. 2015 6 7658 10.1038/ncomms8658
Carrera D.A. George G.M. Fischer-Stettler M. Galbier F. Eicke S. Truernit E. Streb S. Zeeman S.C. Distinct plastid fructose bisphosphate aldolases function in photosynthetic and non-photosynthetic metabolism in Arabidopsis J. Exp. Bot. 2021 72 3739 3755 10.1093/jxb/erab099
Shi J. Yi K. Liu Y. Xie L. Zhou Z. Chen Y. Hu Z. Zheng T. Liu R. Chen Y. et al. Phosphoenolpyruvate Carboxylase in Arabidopsis Leaves Plays a Crucial Role in Carbon and Nitrogen Metabolism Plant Physiol. 2015 167 671 681 10.1104/pp.114.254474
Kim T. Samraj S. Juan Jiménez J. Gómez C. Liu T. Begcy K. Genome-wide identification of heat shock factors and heat shock proteins in response to UV and high intensity light stress in lettuce BMC Plant Biol. 2021 21 185 10.1186/s12870-021-02959-x 33865315
Volkov R.A. Panchuk I. Mullineaux P.M. Schöffl F. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis Plant Mol. Biol. 2006 61 733 746 10.1007/s11103-006-0045-4 16897488
Driedonks N. Xu J. Peters J.L. Park S. Ivo Rieu I. Multi-Level Interactions between Heat Shock Factors, Heat Shock Proteins, and the Redox System Regulate Acclimation to Heat Front. Plant Sci. 2015 6 999 10.3389/fpls.2015.00999 26635827
Hetz C. Zhang K. Kaufman R.J. Mechanisms, regulation and functions of the unfolded protein response Nat. Rev. Mol. Cell Biol. 2020 21 421 438 10.1038/s41580-020-0250-z
Hennessy F. Nicoll W.S. Zimmermann R. Cheetham M.E. Blatch G.L. Not all J domains are created equal: Implications for the specificity of Hsp40-Hsp70 interactions Protein Sci. 2005 14 1697 1709 10.1110/ps.051406805
Kampinga H.H. Craig E.A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity Nat. Rev. Mol. Cell Biol. 2010 11 579 592 10.1038/nrm2941
Pobre K.F.R. Poet G.J. Hendershot L.M. The endoplasmic reticulum (ER) chaperone BiP is a master regulator of ER functions: Getting by with a little help from ERdj friends J. Biol. Chem. 2019 294 2098 2108 10.1074/jbc.REV118.002804
Anken E. Braakman I. Craig E. Versatility of the endoplasmic reticulum protein folding factory Crit. Rev. Biochem. Mol. 2005 40 191 228 10.1080/10409230591008161
Lu D.P. Christopher D.A. Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana Mol. Genet. Genom. 2008 280 199 210 10.1007/s00438-008-0356-z
Irfan M. Kumar P. Ahmad I. Datta A. Unraveling the role of tomato Bcl-2-associated athanogene (BAG) proteins during abiotic stress response and fruit ripening Sci. Rep. 2021 11 21734 10.1038/s41598-021-01185-7 34741097
Sengupta D. Naik D. Reddy A.R. Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: A structure-function update J. Plant Physiol. 2015 179 40 55 10.1016/j.jplph.2015.03.004 25840343
Tiwari P. Chakrabarty D. Dehydrin in the past four decades: From chaperones to transcription co-regulators in regulating abiotic stress response Curr. Res. Biotechnol. 2021 3 249 259 10.1016/j.crbiot.2021.07.005
Puhakainen T. Hess M.W. Mäkelä P. Svensson J. Heino P. Tapio P.E. Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis Plant Mol. Biol. 2004 54 743 753 10.1023/B:PLAN.0000040903.66496.a4 15356392
Kim J.Y. Park S.J. Jang B. Jung C.H. Ahn S.J. Goh C.H. Cho K. Han O. Kang H. Functional characterization of a glycine-rich RNA-binding protein 2 in Arabidopsis thaliana under abiotic stress conditions Plant J. 2007 50 439 451 10.1111/j.1365-313X.2007.03057.x 17376161
Gu L. Jung H.J. Kim B.M. Xu T. Lee K. Kim Y.-O. Kang H. A chloroplast-localized S1 domain-containing protein SRRP1 plays a role in Arabidopsis seedling growth in the presence of ABA J. Plant Physiol. 2015 189 34 41 10.1016/j.jplph.2015.10.003
Finkina E.I. Melnikova D.N. Bogdanov I.V. Ovchinnikova T.V. Lipid Transfer Proteins as Components of the Plant Innate Immune System: Structure, Functions, and Applications Acta Nat. 2016 8 47 61 10.32607/20758251-2016-8-2-47-61
Jülke S. Müller-Ludwig J. Response of Arabidopsis thaliana Roots with Altered Lipid Transfer Protein (LTP) Gene Expression to the Clubroot Disease and Salt Stress Plants 2016 5 2 10.3390/plants5010002
Kanehisa M. Miho Furumichi M. Tanabe M. Sato Y. Morishima K. KEGG: New perspectives on genomes, pathways, diseases and drugs Nucl. Acids Res. 2017 45 D353 D361 10.1093/nar/gkw1092
Gupta K.J. Igamberdiev A.U. The anoxic plant mitochondrion as a nitrite: NO reductase Mitochondrion 2011 11 537 543 10.1016/j.mito.2011.03.005 21406251
Bender D. Schwarz G. Nitrite-dependent nitric oxide synthesis by molybdenum enzymes FEBS Lett. 2018 592 2126 2139 10.1002/1873-3468.13089 29749013
Kolbert Z. Barroso J.B. Brouquisse R. Corpas F.J. Gupta K.J. Lindermayr C. Loake G.J. Palma J.M. Petrivalský M. Wendehenne D. et al. A forty-year journey: The generation and roles of NO in plants Nitric Oxide 2019 93 53 70 10.1016/j.niox.2019.09.006
Gao Z. Chung E.H. Eitas T.K. Dangl J.L. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane Proc. Natl. Acad. Sci. USA 2011 108 7619 7624 10.1073/pnas.1104410108
Paila Y.D. Richardson L.G.L. Schnell D.J. New insights into the mechanism of chloroplast protein import and its integration with protein quality control, organelle biogenesis and development J. Mol. Biol. 2015 427 1038 1060 10.1016/j.jmb.2014.08.016
Bédard J. Trösch R. Wu F. Ling Q. Flores-Pérez Ú. Töpel M. Nawaz F. Paul Jarvis P. Suppressors of the Chloroplast Protein Import Mutant tic40 Reveal a Genetic Link between Protein Import and Thylakoid Biogenesis Plant Cell 2017 29 1726 1747 10.1105/tpc.16.00962
Samol I. Rossig C. Buhr F. Springer A. Pollmann S. Lahroussi A. von Wettstein D. Reinbothe C. Reinbothe S. The outer chloroplast envelope protein OEP16-1 for plastid import of NADPH:protochlorophyllide oxidoreductase A in Arabidopsis thaliana Plant Cell Physiol. 2011 52 96 111 10.1093/pcp/pcq177
Lister R. Carrie C. Duncan O. Ho L.H. Howell K.A. Murcha M.W. Whelan J. Functional definition of outer membrane proteins involved in preprotein import into mitochondria Plant Cell 2007 19 3739 3759 10.1105/tpc.107.050534
Das A. Pramanik K. Sharma R. Gantait S. Banerjee J. In-silico study of biotic and abiotic stress-related transcription factor binding sites in the promoter regions of rice germin-like protein genes PLoS ONE 2019 14 e0211887 10.1371/journal.pone.0211887
Ma L. Cheng K. Li J. Deng Z. Zhang C. Zhu H. Roles of Plant Glycine-Rich RNA-Binding Proteins in Development and Stress Responses Int. J. Mol. Sci. 2021 22 5849 10.3390/ijms22115849 34072567
Rapala-Kozik M. Wolak N. Kujda M. Banas A.K. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response BMC Plant Biol. 2012 12 2 10.1186/1471-2229-12-2 22214485
Xu J. Tian Y.-S. Xing X.-J. Peng R.-H. Zhu B. Gao J.-J. Yao Q.-H. Over-expression of AtGSTU19 provides tolerance to salt, drought and methyl viologen stresses in Arabidopsis Physiol. Plantarum. 2016 156 164 175 10.1111/ppl.12347 25975461
Kriegshauser L. Knosp S. Grienenberger E. Tatsumi K. Gütle D.D. Sørensen I. Herrgott L. Zumsteg J. Rose J.K.C. Reski R. et al. Function of the HYDROXYCINNAMOYL-CoA:SHIKIMATE HYDROXYCINNAMOYL TRANSFERASE is evolutionarily conserved in embryophytes Plant Cell 2021 33 1472 1491 10.1093/plcell/koab044
Ye N. Zhu G. Liu Y. Yingxuan L. Zhang J. ABA Controls H2O2 Accumulation Through the Induction of OsCATB in Rice Leaves Under Water Stress Plant Cell Physiol. 2011 52 689 698 10.1093/pcp/pcr028
de Dios A. A concise appraisal of lipid oxidation and lipoxidation in higher plants Redox Biol. 2019 23 101136 10.1016/j.redox.2019.101136
Biswas M.S. Mano J. Lipid Peroxide-Derived Short-Chain Carbonyls Mediate Hydrogen Peroxide-Induced and Salt-Induced Programmed Cell Death in Plants Plant Physiol. 2015 168 885 898 10.1104/pp.115.256834
Costa-Broseta Á. Castillo M. León J. Nitrite Reductase 1 Is a Target of Nitric Oxide-Mediated Post-Translational Modifications and Controls Nitrogen Flux and Growth in Arabidopsis Int. J. Mol. Sci. 2020 21 7270 10.3390/ijms21197270
Christen P. Han W. Cis-Effect of DnaJ on DnaK in ternary complexes with chimeric DnaK/DnaJ-binding peptides FEBS Lett. 2004 563 146 150 10.1016/S0014-5793(04)00290-X
Cavieres L.A. Vivas M. Mihoc M.A.K. Osses D.A. Ortiz-Gutiérrez J.M. Sáez P. Bravo L.A. The importance of facilitative interactions on the performance of Colobanthus quitensis in an Antarctic tundra J. Veg. Sci. 2018 29 236 244 10.1111/jvs.12616
Perez-Riverol Y. Bai J. Bandla C. Hewapathirana S. García-Seisdedos D. Kamatchinathan S. Kundu D. Prakash A. Frericks-Zipper A. Eisenacher M. et al. The PRIDE database resources in 2022: A Hub for mass spectrometry-based proteomics evidences Nucleic Acids Res. 2022 50 D543 D552 10.1093/nar/gkab1038 34723319
Szklarczyk D. Morris J.H. Cook H. Kuhn M. Wyder S. Simonovic M. The STRING database in 2017: Quality-controlled protein-protein association networks, made broadly accessible Nucleic Acids Res. 2017 45 D362 D368 10.1093/nar/gkw937 27924014
Bertini L. Focaracci F. Proietti S. Papetti P. Caruso C. Physiological response of Posidonia oceanica to heavy metal pollution along the Tyrrhenian coast Funct. Plant Biol. 2019 46 933 941 10.1071/FP18303 31186089
Bradford M.M. A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of 778 protein-dye binding Anal. Biochem. 1976 72 248 254 10.1016/0003-2697(76)90527-3
Claiborne A. Catalase activity Handbook of Methods for Oxygen Radical Research Greenwald R.A. CRC Press Boca Raton, FL, USA 1984 283 284
Proietti S. Bertini L. Falconieri G.S. Baccelli I. Timperio A.M. Caruso C. A Metabolic Profiling Analysis Revealed a Primary Metabolism Reprogramming in Arabidopsis glyI4 Loss-of-Function Mutant Plants 2021 10 2464 10.3390/plants10112464 34834827
Bertini L. Proietti S. Focaracci F. Canini F. Bravo L.A. Rabert C. Caruso C. Identification and validation of new reference genes for accurate qRT-PCR normalization in the Antarctic plant Colobanthus quitensis under abiotic stress conditions Polar Biol. 2021 44 389 405 10.1007/s00300-021-02801-y