The resurrection plant Ramonda serbica Panc. survives long desiccation periods and fully recovers metabolic functions within one day upon watering. This study aimed to identify key candidates and pathways involved in desiccation tolerance in R. serbica. We combined differential transcriptomics and proteomics, phenolic and sugar analysis, FTIR analysis of the cell wall polymers, and detailed analysis of the photosynthetic electron transport (PET) chain. The proteomic analysis allowed the relative quantification of 1192 different protein groups, of which 408 were differentially abundant between hydrated (HL) and desiccated leaves (DL). Almost all differentially abundant proteins related to photosynthetic processes were less abundant, while chlorophyll fluorescence measurements implied shifting from linear PET to cyclic electron transport (CET). The levels of H2O2 scavenging enzymes, ascorbate-glutathione cycle components, catalases, peroxiredoxins, Fe-, and Mn superoxide dismutase (SOD) were reduced in DL. However, six germin-like proteins (GLPs), four Cu/ZnSOD isoforms, three polyphenol oxidases, and 22 late embryogenesis abundant proteins (LEAPs; mainly LEA4 and dehydrins), were desiccation-inducible. Desiccation provoked cell wall remodeling related to GLP-derived H2O2/HO● activity and pectin demethylesterification. This comprehensive study contributes to understanding the role and regulation of the main metabolic pathways during desiccation aiming at crop drought tolerance improvement.

Biology Center of the Czech Academy of Sciences Institute of Plant Molecular Biology Department of Plant Biophysics and Biochemistry Branišovska 31 1160 370 05 Ceske Budejovice Czech Republic

Department of Agronomy Food Natural Resources Animals and Environment University of Padova Viale dell'Università 16 35020 Legnaro Italy

Department of Biomedical Sciences University of Padova Via Ugo Bassi 58 B 35131 Padova Italy

Institute for Multidisciplinary Research Department of Life Science University of Belgrade Kneza Viseslava 1 11000 Belgrade Serbia

Institute of Molecular Genetics and Genetic Engineering Laboratory for Plant Molecular Biology University of Belgrade Vojvode Stepe 444a 11042 Belgrade Serbia

Proteomics Center University of Padova and Azienda Ospedaliera di Padova Via G Orus 2 B 35129 Padova Italy

See more in PubMed

Rabara R.C., Tripathi P., Reese R.N., Rushton D.L., Alexander D., Timko M.P., Rushton P.J. Tobacco drought stress responses reveal new targets for Solanaceae crop improvement. BMC Genom. 2015;16:484. doi: 10.1186/s12864-015-1575-4. PubMed DOI PMC

Farrant J.M., Hilhorst H.W.M. What is dry? Exploring metabolism and molecular mobility at extremely low water contents. J. Exp. Bot. 2021;72:1507–1510. doi: 10.1093/jxb/eraa579. PubMed DOI PMC

Challabathula D., Zhang Q., Bartels D. Protection of photosynthesis in desiccation-tolerant resurrection plants. J. Plant Physiol. 2018;227:84–92. doi: 10.1016/j.jplph.2018.05.002. PubMed DOI

Scott P. Resurrection plants and the secrets of eternal leaf. Ann. Bot. 2000;85:159–166. doi: 10.1006/anbo.1999.1006. DOI

Veljović-Jovanović S., Kukavica B., Stevanović B., Navari-Izzo F. Senescence-and drought-related changes in peroxidase and superoxide dismutase isoforms in leaves of Ramonda serbica. J. Exp. Bot. 2006;57:1759–1768. doi: 10.1093/jxb/erl007. PubMed DOI

Challabathula D., Bartels D. Desiccation tolerance in resurrection plants: New insights from transcriptome, proteome and metabolome analysis. Front. Plant Sci. 2013;4:482–497. PubMed PMC

Liu J., Moyankova D., Lin C.T., Mladenov P., Sun R.Z., Djilianov D., Deng X. Transcriptome reprogramming during severe dehydration contributes to physiological and metabolic changes in the resurrection plant Haberlea rhodopensis. BMC Plant Biol. 2018;18:351–367. doi: 10.1186/s12870-018-1566-0. PubMed DOI PMC

Farrant J.M., Moore J.P. Programming desiccation-tolerance: From plants to seeds to resurrection plants. Curr. Opin. Plant Biol. 2011;14:340–345. doi: 10.1016/j.pbi.2011.03.018. PubMed DOI

Chandra J., Keshavkant S. Desiccation-induced ROS accumulation and lipid catabolism in recalcitrant. Physiol. Mol. Biol. Plants. 2018;24:75–87. doi: 10.1007/s12298-017-0487-y. PubMed DOI PMC

Gechev T.S., Dinakar C., Benina M., Toneva V., Bartels D. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell. Mol. Life Sci. 2012;69:3175–3186. doi: 10.1007/s00018-012-1088-0. PubMed DOI PMC

Bartels D. Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr. Comp. Biol. 2005;45:696–701. doi: 10.1093/icb/45.5.696. PubMed DOI

Olvera-Carrillo Y., Campos F., Reyes J.L., Garciarrubio A., Covarrubias A.A. Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol. 2010;154:373–390. doi: 10.1104/pp.110.158964. PubMed DOI PMC

Farrant J.M. Mechanisms of desiccation tolerance in angiosperm resurrection plants. Plant Stress. 2007;1:72–84.

Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim. Biophys. Acta–Bioenerg. 2010;1797:1313–1326. doi: 10.1016/j.bbabio.2010.03.008. PubMed DOI

Dirk L.M.A., Abdel C.G., Ahmad I., Neta I.C.S., Pereira C.C., Pereira F.E.C.B., Unêda-Trevisoli S.H., Pinheiro D.G., Downie A.B. Late embryogenesis abundant protein-client protein interactions. Plants. 2020;9:814. doi: 10.3390/plants9070814. PubMed DOI PMC

Ginsawaeng O., Heise C., Sangwan R., Karcher D., Hernández-Sánchez I.E., Sampathkumar A., Zuther E. Subcellular localization of seed-expressed LEA_4 proteins reveals liquid-liquid phase separation for LEA9 and for LEA48 homo- and LEA42-LEA48 heterodimers. Biomolecules. 2021;11:1770. doi: 10.3390/biom11121770. PubMed DOI PMC

Dražić G., Mihailović N., Stevanović B. Chlorophyll metabolism in leaves of higher poikilohydric plants Ramonda serbica Panč. and Ramonda nathaliae Panč. et Petrov. during dehydration and rehydration. J. Plant Physiol. 1999;154:379–384. doi: 10.1016/S0176-1617(99)80184-9. DOI

Zhu Y., Wang B., Phillips J., Zhang Z.N., Du H., Xu T., Huang L.C., Zhang X.F., Xu G.H., Li W.L., et al. Global transcriptome analysis reveals acclimation–primed processes involved in the acquisition of desiccation tolerance in Boea hygrometrica. Plant Cell Physiol. 2015;56:1429–1441. doi: 10.1093/pcp/pcv059. PubMed DOI

Artur M.A.S., Zhao T., Ligterink W., Schranz E., Hilhorst H.W.M. Dissecting the genomic diversification of late embryogenesis abundant (LEA) protein gene families in plants. Genome Biol. Evol. 2019;11:459–471. doi: 10.1093/gbe/evy248. PubMed DOI PMC

Thimm O., Bläsing O., Gibon Y., Nagel A., Meyer S., Krüger P., Stitt M. MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004;37:914–939. doi: 10.1111/j.1365-313X.2004.02016.x. PubMed DOI

Pantelić A., Stevanović S., Komić S.M., Kilibarda N., Vidović M. In silico characterisation of the late embryogenesis abundant (LEA) protein families and their role in desiccation tolerance in Ramonda serbica Panc. Int. J. Mol. Sci. 2022;23:3547. doi: 10.3390/ijms23073547. PubMed DOI PMC

Živanović B., Milić-Komić S., Nikolić N., Mutavdžić D., Srećković T., Veljović-Jovanović S., Prokić L. Differential response of two tomato genotypes, wild type cv. Ailsa Craig and its ABA-deficient mutant flacca to short-termed drought cycles. Plants. 2021;10:2308. doi: 10.3390/plants10112308. PubMed DOI PMC

Alonso-Simón A., García-Angulo P., Mélida H., Encina A., Álvarez J.M., Acebes J.L. The use of FTIR spectroscopy to monitor modifications in plant cell wall architecture caused by cellulose biosynthesis inhibitors. Plant Signal. Behav. 2011;6:1104–1110. doi: 10.4161/psb.6.8.15793. PubMed DOI PMC

Ross A.B., Langer J.D., Jovanovic M. Proteome turnover in the spotlight: Approaches, applications, and perspectives. Mol. Cell. Proteom. 2021;20:100016. doi: 10.1074/mcp.R120.002190. PubMed DOI PMC

Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012;13:227–232. doi: 10.1038/nrg3185. PubMed DOI PMC

Fernie A.R., Stitt M. On the discordance of metabolomics with proteomics and transcriptomics: Coping with increasing complexity in logic, chemistry, and network interactions scientific correspondence. Plant Physiol. 2012;158:1139–1145. doi: 10.1104/pp.112.193235. PubMed DOI PMC

Liang C., Cheng S., Zhang Y., Sun Y., Fernie A.R., Kang K., Panagiotou G., Lo C., Lim B.L. Transcriptomic, proteomic and metabolic changes in Arabidopsis thaliana leaves after the onset of illumination. BMC Plant Biol. 2016;16:43. doi: 10.1186/s12870-016-0726-3. PubMed DOI PMC

Xu X., Legay S., Sergeant K., Zorzan S., Leclercq C.C., Charton S., Giarola V., Liu X., Challabathula D., Renaut J., et al. Molecular insights into plant desiccation tolerance: Transcriptomics, proteomics and targeted metabolite profiling in Craterostigma plantagineum. Plant J. 2021;107:377–398. doi: 10.1111/tpj.15294. PubMed DOI PMC

Rakić T., Lazarević M., Jovanović Z.S., Radović S., Siljak–Yakovlev S., Stevanović B., Stevanović V. Resurrection plants of the genus Ramonda: Prospective survival strategies—Unlock further capacity of adaptation, or embark on the path of evolution? Front. Plant Sci. 2014;4:550–560. doi: 10.3389/fpls.2013.00550. PubMed DOI PMC

Moore J.P., Nguema-Ona E.E., Vicré-Gibouin M., Sørensen I., Willats W.G., Driouich A., Farrant J.M. Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta. 2013;237:739–754. doi: 10.1007/s00425-012-1785-9. PubMed DOI

Jung N.U. Ph.D. Thesis. Mathematisch-Naturwissenschaftlichen Fakultät, Rheinischen Friedrich-Wilhelms-Universität Bonn; Bonn, Germany: Feb 11, 2020. Molecular and Biochemical Studies of the Craterostigma plantagineum Cell Wall during Dehydration and Rehydration.

Vicré M., Lerouxel O., Farrant J., Lerouge P., Driouich A. Composition and desiccation-induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii. Physiol. Plant. 2004;120:229–239. doi: 10.1111/j.0031-9317.2004.0234.x. PubMed DOI

Wormit A., Usadel B. The multifaceted role of pectin methylesterase inhibitors (PMEIs) Int. J. Mol. Sci. 2018;19:2878. doi: 10.3390/ijms19102878. PubMed DOI PMC

Jung N.U., Giarola V., Chen P., Knox J.P., Bartels D. Craterostigma plantagineum cell wall composition is remodelled during desiccation and the glycine-rich protein CpGRP1 interacts with pectins through clustered arginines. Plant J. 2019;100:661–676. doi: 10.1111/tpj.14479. PubMed DOI

Levesque-Tremblay G., Pelloux J., Braybrook S.A., Müller K. Tuning of pectin methylesterification: Consequences for cell wall biomechanics and development. Planta. 2015;242:791–811. doi: 10.1007/s00425-015-2358-5. PubMed DOI

Wang L., Shang H., Liu Y., Zheng M., Wu R., Phillips J., Bartels D., Deng X. A role for a cell wall localized glycine-rich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol. 2009;11:837–848. doi: 10.1111/j.1438-8677.2008.00187.x. PubMed DOI

Giarola V., Krey S., von den Driesch B., Bartels D. The Craterostigma plantagineum glycine-rich protein CpGRP1 interacts with a cell wall-associated protein kinase 1 (CpWAK1) and accumulates in leaf cell walls during dehydration. New Phytol. 2016;210:535–550. doi: 10.1111/nph.13766. 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;10:583–601. doi: 10.3389/fpls.2019.00583. PubMed DOI PMC

Veljović-Jovanović S., Kukavica B., Vidović M., Morina F., Menckhoff L. Class III peroxidases: Functions, localization and redox regulation of isoenzymes. In: Gupta D.K., Palma J.M., Corpas F.J., editors. Antioxidants and Antioxidant Enzymes in Higher Plants. Springer; Cham, Switzerland: New York, NY, USA: 2018. pp. 269–300.

Pristov J.B., Mitrović A., Spasojević I. A comparative study of antioxidative activities of cell-wall polysaccharides. Carbohydr. Res. 2011;346:2255–2259. doi: 10.1016/j.carres.2011.07.015. PubMed DOI

Kukavica B., Mojović M., Vučinić Ž., Maksimović V., Takahama U., Veljović-Jovanović S. Generation of hydroxyl radical in isolated pea root cell wall, and the role of cell wall-bound peroxidase, Mn-SOD and phenolics in their production. Plant Cell Physiol. 2009;50:304–317. doi: 10.1093/pcp/pcn199. PubMed DOI

Collett H.M., Butowt R., Smith J., Farrant J., Illing N. Photosynthetic genes are differentially transcribed during the dehydration-rehydration cycle in the resurrection plant, Xerophyta humilis. J. Exp. Bot. 2003;54:2543–2595. doi: 10.1093/jxb/erg285. PubMed DOI

Yang E.J., Oh Y.A., Lee E.S., Park A.R., Cho S.K., Yoo Y.J., Park O.K. Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem. Biophys. Res. Commun. 2003;305:862–868. doi: 10.1016/S0006-291X(03)00851-9. PubMed DOI

Jiang G., Wang Z., Shang H., Yang W., Hu Z., Phillips J., Deng X. Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta. 2007;225:1405–1420. doi: 10.1007/s00425-006-0449-z. PubMed DOI

Farrant J.M. A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol. 2000;151:29–39. doi: 10.1023/A:1026534305831. DOI

Heber U., Bilger W., Bligny R., Lange O.L. Photo-tolerance of lichens, mosses and higher plants in an alpine environment: Analysis of photoreactions. Planta. 2000;211:770–780. doi: 10.1007/s004250000356. PubMed DOI

Huang W., Yang S.-J., Zhang S.-B., Zhang J.-L., Cao K.-F. Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta. 2012;235:819–828. doi: 10.1007/s00425-011-1544-3. PubMed DOI

Tan T., Sun Y., Luo S., Zhang C., Zhou H., Lin H. Efficient modulation of photosynthetic apparatus confers desiccation tolerance in the resurrection plant Boea hygrometrica. Plant Cell Physiol. 2017;58:1976–1990. doi: 10.1093/pcp/pcx140. PubMed DOI

Mladenov P., Finazzi G., Bligny R., Moyankova D., Zasheva D., Boisson A.-M., Brugière S., Krasteva V., Alipieva K., Simova S., et al. In vivo spectroscopy and NMR metabolite fingerprinting approaches to connect the dynamics of photosynthetic and metabolic phenotypes in resurrection plant Haberlea rhodopensis during desiccation and recovery. Front. Plant Sci. 2015;6:564–578. doi: 10.3389/fpls.2015.00564. PubMed DOI PMC

Markovska Y., Tsonev T., Kimenov G. Regulation of cam and respiratory recycling by water supply in higher poikilohydric plants—Haberlea rhodopensis Friv. and Ramonda serbica Panc, at transition from biosis to anabiosis and vice versa. Bot. Acta. 1997;110:18–24. doi: 10.1111/j.1438-8677.1997.tb00606.x. DOI

Kirch H.H., Nair A., Bartels D. Novel ABA-and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. Plant J. 2001;28:555–567. doi: 10.1046/j.1365-313X.2001.01176.x. PubMed DOI

Živković T., Quartacci M.F., Stevanović B., Marinone F., Navari-Izzo F. Low molecular weight substances in the poikilohydric plant Ramonda serbica during dehydration and rehydration. Plant Sci. 2005;168:105–111. doi: 10.1016/j.plantsci.2004.07.018. DOI

Ingram J., Bartels D. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. 1996;47:377–403. doi: 10.1146/annurev.arplant.47.1.377. PubMed DOI

Vidović M., Morina F., Milić S., Albert A., Zechmann B., Tosti T., Winkler J.B., Jovanović S.V. Carbon allocation from source to sink leaf tissue in relation to flavonoid biosynthesis in variegated Pelargonium zonale under UV-B radiation and high PAR intensity. Plant Physiol. Biochem. 2015;93:44–55. doi: 10.1016/j.plaphy.2015.01.008. PubMed DOI

Nishizawa A., Yabuta Y., Shigeoka S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008;147:1251–1263. doi: 10.1104/pp.108.122465. PubMed DOI PMC

Dietz K.J., Jacob S., Oelze M.L., Laxa M., Tognetti V., de Miranda S.M., Baier M., Finkemeier I. The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 2016;57:1697–1709. doi: 10.1093/jxb/erj160. PubMed DOI

Augusti A., Scartazza A., Navari-Izzo F., Sgherri C.L.M., Stevanović B., Brugnoli E. Photosystem II photochemical efficiency, zeaxanthin and antioxidant contents in the poikilohydric Ramonda serbica during dehydration and rehydration. Photosynth. Res. 2001;67:79–88. doi: 10.1023/A:1010692632408. PubMed DOI

Vidović M., Franchin C., Morina F., Veljović-Jovanović S., Masi A., Arrigoni G. Efficient protein extraction for shotgun proteomics from hydrated and desiccated leaves of resurrection Ramonda serbica plants. Anal. Bioanal. Chem. 2020;412:8299–8312. doi: 10.1007/s00216-020-02965-2. PubMed DOI

Vidović M., Morina F., Veljović-Jovanović S. Stimulation of various phenolics in plants under ambient UV-B radiation. In: Singh V.P., Singh S., Prasad S.M., Parihar P., editors. UV-B Radiation: From Environmental Stressor to Regulator of Plant Growth. Wiley-Blackwell; Hoboken, NJ, USA: 2017. pp. 9–56.

Veljović-Jovanović S., Kukavica B., Navari-Izzo F. Characterization of polyphenol oxidase changes induced by desiccation of Ramonda serbica leaves. Physiol. Plant. 2008;132:407–416. doi: 10.1111/j.1399-3054.2007.01040.x. PubMed DOI

Sgherri C., Stevanovic B., Navari-Izzo F. Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol. Plant. 2004;122:478–485. doi: 10.1111/j.1399-3054.2004.00428.x. DOI

Takahama U. Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: Physiological significance of the oxidation reactions. Phytochem. Rev. 2004;3:207–219. doi: 10.1023/B:PHYT.0000047805.08470.e3. DOI

Boeckx T., Winters A.L., Webb K.J., Kingston-Smith A.H. Polyphenol oxidase in leaves: Is there any significance to the chloroplastic localization? J. Exp. Bot. 2015;66:3571–3579. doi: 10.1093/jxb/erv141. PubMed DOI

Bremer A., Wolff M., Thalhammer A., Hincha D.K. Folding of intrinsically disordered plant LEA proteins is driven by glycerol-induced crowding and the presence of membranes. FEBS J. 2017;284:919–936. doi: 10.1111/febs.14023. PubMed DOI

Cuevas-Velazquez C.L., Reyes J.L., Covarrubias A.A. Group 4 late embryogenesis abundant proteins as a model to study intrinsically disordered proteins in plants. Plant Signal. Behav. 2017;12:10893–10903. doi: 10.1080/15592324.2017.1343777. PubMed DOI PMC

Candat A., Paszkiewicz G., Neveu M., Gautier R., Logan D.C., Avelange-Macherel M.H., Macherel D. The ubiquitous distribution of late embryogenesis abundant proteins across cell compartments in Arabidopsis offers tailored protection against abiotic stress. Plant Cell. 2014;26:3148–3166. doi: 10.1105/tpc.114.127316. PubMed DOI PMC

Koag M.C., Wilkens S., Fenton R.D., Resnik J., Vo E., Close T.J. The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol. 2009;150:1503–1514. doi: 10.1104/pp.109.136697. PubMed DOI PMC

Hara M., Shinoda Y., Tanaka Y., Kuboi T. DNA binding of citrus dehydrin promoted by zinc ion. Plant Cell Environ. 2009;32:532–541. doi: 10.1111/j.1365-3040.2009.01947.x. PubMed DOI

Liu X., Wang Z., Wang L., Wu R., Phillips J., Deng X. LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Sci. 2009;176:90–98. doi: 10.1016/j.plantsci.2008.09.012. DOI

Olvera-Carrillo Y., Luis Reyes J., Covarrubias A.A. Late embryogenesis abundant proteins: Versatile players in the plant adaptation to water limiting environments. Plant Signal. Behav. 2011;6:586–589. doi: 10.4161/psb.6.4.15042. PubMed DOI PMC

Chakrabortee S., Tripathi R., Watson M., Schierle G.S., Kurniawan D.P., Kaminski C.F., Wise M.J., Tunnacliffe A. Intrinsically disordered proteins as molecular shields. Mol. Biosyst. 2012;8:210–219. doi: 10.1039/C1MB05263B. PubMed DOI PMC

Belott C., Janis B., Menze M.A. Liquid-liquid phase separation promotes animal desiccation tolerance. Proc. Natl. Acad. Sci. USA. 2020;117:27676–27684. doi: 10.1073/pnas.2014463117. PubMed DOI PMC

Rohrig H., Schmidt J., Colby T., Brautigam A., Hufnagel P., Bartels D. Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation. Plant Cell Environ. 2006;29:1606–1617. doi: 10.1111/j.1365-3040.2006.01537.x. PubMed DOI

Biundo A., Braunschmid V., Pretzler M., Kampatsikas I., Darnhofer B., Birner-Gruenberger R., Rompel A., Ribitsch D., Guebitz G.M. Polyphenol oxidases exhibit promiscuous proteolytic activity. Commun. Chem. 2020;3:62. doi: 10.1038/s42004-020-0305-2. PubMed DOI PMC

Harten J.B., Eickmeier W.G. Enzyme dynamics of the resurrection plant Selaginella lepidophylla (Hook. & Grev.) spring during rehydration. Plant Phys. 1986;82:61–64. PubMed PMC

Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Ebinezer L.B., Franchin C., Trentin A.R., Carletti P., Trevisan S., Agrawal G.K., Quaggiotti S., Arrigoni G., Masi A. Quantitative proteomics of maize roots treated with a protein hydrolysate: A comparative study with transcriptomics highlights the molecular mechanisms responsive to biostimulants. J. Agric. Food Chem. 2020;68:7541–7553. doi: 10.1021/acs.jafc.0c01593. PubMed DOI

Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007;2:953–971. doi: 10.1038/nprot.2007.131. PubMed DOI

Küpper H., Benedikty Z., Morina F., Andresen E., Mishra A., Trtilek M. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant Physiol. 2019;179:369–381. doi: 10.1104/pp.18.00953. PubMed DOI PMC

Lichtenthaler H.K., Wellburn A.R. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 1983;11:591–592. doi: 10.1042/bst0110591. DOI