The disadvantages of being a hybrid during drought: A combined analysis of plant morphology, physiology and leaf proteome in maize

. 2017 ; 12 (4) : e0176121. [epub] 20170418

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28419152

A comparative analysis of various parameters that characterize plant morphology, growth, water status, photosynthesis, cell damage, and antioxidative and osmoprotective systems together with an iTRAQ analysis of the leaf proteome was performed in two inbred lines of maize (Zea mays L.) differing in drought susceptibility and their reciprocal F1 hybrids. The aim of this study was to dissect the parent-hybrid relationships to better understand the mechanisms of the heterotic effect and its potential association with the stress response. The results clearly showed that the four examined genotypes have completely different strategies for coping with limited water availability and that the inherent properties of the F1 hybrids, i.e. positive heterosis in morphological parameters (or, more generally, a larger plant body) becomes a distinct disadvantage when the water supply is limited. However, although a greater loss of photosynthetic efficiency was an inherent disadvantage, the precise causes and consequences of the original predisposition towards faster growth and biomass accumulation differed even between reciprocal hybrids. Both maternal and paternal parents could be imitated by their progeny in some aspects of the drought response (e.g., the absence of general protein down-regulation, changes in the levels of some carbon fixation or other photosynthetic proteins). Nevertheless, other features (e.g., dehydrin or light-harvesting protein contents, reduced chloroplast proteosynthesis) were quite unique to a particular hybrid. Our study also confirmed that the strategy for leaving stomata open even when the water supply is limited (coupled to a smaller body size and some other physiological properties), observed in one of our inbred lines, is associated with drought-resistance not only during mild drought (as we showed previously) but also during more severe drought conditions.

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Chen ZJ. Genomic and epigenetic insights into the molecular bases of heterosis. Nature Rev Genet. 2013;14: 471–482. 10.1038/nrg3503 PubMed DOI

Fu D, Xiao M, Hayward A, Jiang G, Zhu L, Zhou Q, et al. What is crop heterosis: new insights into an old topic. J Appl Genet. 2015;56: 1–13. 10.1007/s13353-014-0231-z PubMed DOI

Baranwal VK, Mikkilineni V, Zehr UB, Tyagi AK, Kapoor S. Heterosis: emerging ideas about hybrid vigour. J Exp Bot. 2012;63: 6309–6314. 10.1093/jxb/ers291 PubMed DOI

Goff SA, Zhang Q. Heterosis in elite hybrid rice: speculation on the genetic and biochemical mechanisms. Curr Opin Plant Biol. 2013;16: 221–227. 10.1016/j.pbi.2013.03.009 PubMed DOI

Paschold A, Marcon C, Hoecker N, Hochholdinger F. Molecular dissection of heterosis manifestation during early maize root development. Theor Appl Genet. 2010;120: 383–388. 10.1007/s00122-009-1082-6 PubMed DOI

Xing J, Sun Q, Ni Z. Proteomic patterns associated with heterosis. Biochim Biophys Acta—Proteins Proteomics. 2016;1864: 908–915. PubMed

Marcon C, Schützenmeister A, Schütz W, Madlung J, Piepho HP, Hochholdinger F. Nonadditive protein accumulation patterns in maize (Zea mays L.) hybrids during embryo development. J Proteome Res. 2010;9: 6511–6522. 10.1021/pr100718d PubMed DOI

Fu Z, Jin X, Ding D, Li Y, Fu Z, Tang J. Proteomic analysis of heterosis during maize seed germination. Proteomics. 2011;11: 1462–1472. 10.1002/pmic.201000481 PubMed DOI

Guo B, Chen Y, Zhang G, Xiang J, Hu Z, Feng W, et al. Comparative proteomic analysis of embryos between a maize hybrid and its parental lines during early stages of seed germination. PloS ONE. 2013;8: e65867 10.1371/journal.pone.0065867 PubMed DOI PMC

Wang Z, Xue Z, Wang T. Differential analysis of proteomes and metabolomes reveals additively balanced-networking for metabolism in maize heterosis. J Proteome Res. 2014;13: 3987–4001. 10.1021/pr500337j PubMed DOI

Jin X, Fu Z, Ding D, Li W, Liu Z, Hu Y, et al. Proteomic analysis of plumules and coleoptiles in maize between hybrids and their corresponding inbred lines. Acta Physiol Plant. 2014;36: 355–370.

Dahal D, Mooney BP, Newton KJ. Specific changes in total and mitochondrial proteomes are associated with higher levels of heterosis in maize hybrids. Plant J. 2012;72: 70–83. 10.1111/j.1365-313X.2012.05056.x PubMed DOI

Dahal D, Newton KJ, Mooney BP. Quantitative proteomics of Zea mays hybrids exhibiting different levels of heterosis. J Proteome Res. 2016;15: 2445–2454. 10.1021/acs.jproteome.5b01120 PubMed DOI

Hoecker N, Lemkemeyer T, Sarholz B, Paschold A, Fladerer C, Madlung J, et al. Analysis of nonadditive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines. Proteomics. 2008;8: 3882–3894. 10.1002/pmic.200800023 PubMed DOI

Marcon C, Lamkemeyer T, Malik WA, Ungrue D, Piepho HP, Hochholdinger F. Heterosis-associated proteome analyses of maize (Zea mays L.) seminal roots by quantitative label-free LC-MS. J Proteomics. 2013;93: 295–302. 10.1016/j.jprot.2013.04.015 PubMed DOI

Guo B, Chen Y, Li C, Wang T, Wang R, Wang B, et al. Maize (Zea mays L.) seedling leaf nuclear proteome and differentially expressed proteins between a hybrid and its parental lines. Proteomics. 2014;14: 1071–1087. 10.1002/pmic.201300147 PubMed DOI

Zhang C, Yin Y, Zhang A, Lu Q, Wen X, Zhu Z, et al. Comparative proteomic study reveals dynamic proteome changes between superhybrid rice LYP9 and its parents at different developmental stages. J Plant Physiol. 2012;168: 387–398. PubMed

Song X, Ni Z, Yao Y, Zhang Y, Sun Q. Identification of differentially expressed proteins between hybrid and parents in wheat (Triticum aestivum L.) seedling leaves. Theor Appl Genet. 2009;118: 213–225. 10.1007/s00122-008-0890-4 PubMed DOI

He Q, He H, Deng XW. Epigenetic variation in plant hybrids and their potential roles in heterosis. J Genet Genom. 2013;40: 205–210. PubMed

Adalatzadeh-Aghdam S, Toorchi M, Shakiba MR. Heterosis investigation of sunflower (Helianthus annuus L.) by two-dimensional electrophoresis. Int J Biosci. 2014;4: 70–79.

Mohayeji M, Capriotti AL, Cavaliere C, Piovesana S, Samperi R, Stampachiacchiere S, et al. Heterosis profile of sunflower leaves: a label free proteomics approach. J Proteomics. 2014;99: 101–110. 10.1016/j.jprot.2014.01.028 PubMed DOI

Qin J, Gu F, Liu D, Yin C, Zhao S, Chen H, et al. Proteomic analysis of elite soybean Jidou17 and its parents using iTRAQ-based quantitative approaches. Proteome Sci. 2013;11: 12 10.1186/1477-5956-11-12 PubMed DOI PMC

Han P, Lu X, Mi F, Dong J, Xue C, Li J, et al. Proteomic analysis of heterosis in the leaves of sorghum–sudangrass hybrids. Acta Biochim Biophys Sin. 2016;48: 161–173. 10.1093/abbs/gmv126 PubMed DOI

Blum A. Heterosis, stress, and the environment: a possible road map towards the general improvement of crop yield. J Exp Bot. 2013;64: 4829–4837. 10.1093/jxb/ert289 PubMed DOI

Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature. 2009;457: 327–331. 10.1038/nature07523 PubMed DOI PMC

Ko DK, Rohozinski D, Song Q, Taylor SH, Juenger TE, Harmon FG, et al. Temporal shift of circadian-mediated gene expression and carbon fixation contributes to biomass heterosis in maize hybrids. PLoS Genet. 2016;12: 1006197. PubMed PMC

Groszmann M, Gonzalez-Bayon R, Lyons RL, Greaves IK, Kazan K, Peacock WJ, et al. Hormone-regulated defense and stress response networks contribute to heterosis in Arabidopsis F1 hybrids. Proc Natl Acad Sci USA. 2015;112: E6397–E6406. 10.1073/pnas.1519926112 PubMed DOI PMC

Goff SA. A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol. 2011;189: 923–937. 10.1111/j.1469-8137.2010.03574.x PubMed DOI

Kutík J, Holá D, Kočová M, Rothová O, Haisel D, Wilhelmová N, et al. Ultrastructure and dimensions of chloroplasts in leaves of three maize (Zea mays L.) inbred lines and their F1 hybrids grown under moderate chilling stress. Photosynthetica. 2004;42: 447–455.

Holá D, Langrová K, Kočová M, Rothová O. Photosynthetic parameters of maize (Zea mays L.) inbred lines and F1 hybrids: their different response to, and recovery from rapid or gradual onset of low-temperature stress. Photosynthetica. 2003;41: 429–442.

Holá D, Kočová M, Rothová O, Wilhelmová N, Benešová M. Recovery of maize (Zea mays L.) inbreds and hybrids from chilling stress of various duration: photosynthesis and antioxidant enzymes. J Plant Physiol. 2007;164: 868–877. 10.1016/j.jplph.2006.04.016 PubMed DOI

Kočová M, Holá D, Wilhelmová N, Rothová O. The influence of low-temperature on the photochemical activity of chloroplasts and activity of antioxidant enzymes in maize leaves. Biol Plant. 2009;53: 475–483.

Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES. Heterosis in Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci USA. 2012;109: 7109–7114. 10.1073/pnas.1204464109 PubMed DOI PMC

Rohde P, Hincha D K, Heyer AG. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia‐0 and C24) that show differences in non‐acclimated and acclimated freezing tolerance. Plant J. 2004;38: 790–799. 10.1111/j.1365-313X.2004.02080.x PubMed DOI

Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant. 2010;3: 224–235. 10.1093/mp/ssp105 PubMed DOI PMC

Chen X, Li W, Lu Q, Wen X, Li H, Kuang T, et al. The xanthophyll cycle and antioxidative defense system are enhanced in the wheat hybrid subjected to high light stress. J Plant Physiol. 2011;168: 1828–1836. 10.1016/j.jplph.2011.05.019 PubMed DOI

Yadav OP, Weltzien-Rattunde E, Bidinger FR, Mahalakshmi V. Heterosis in landrace-based topcross hybrids of pearl millet across arid environments. Euphytica. 2000;112: 285–295.

Makumbi D, Betrán JF, Bänziger M, Ribaut JM. Combining ability, heterosis and genetic diversity in tropical maize (Zea mays L.) under stress and non-stress conditions. Euphytica. 2011;180: 143–162.

Blum A, Ramaiah S, Kanemasu ET, Paulsen GM. The physiology of heterosis in sorghum with respect to environmental stress. Ann Bot. 1990;65: 149–158.

Haussmann BIG, Obilana AB, Blum A, Ayiecho PO, Schipprack W, Geiger HH. Hybrid performance of sorghum and its relationship to morphological and physiological traits under variable drought stress in Kenya. Plant Breed. 1998;117: 223–229.

Araus JL, Sánchez C, Cabreba-Bosquet L. Is heterosis in maize mediated through better water use? New Phytol. 2010;187: 392–406. 10.1111/j.1469-8137.2010.03276.x PubMed DOI

Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS. Allelic variation of gene expression in maize hybrids. Plant Cell. 2004;16: 1707–1716. 10.1105/tpc.022087 PubMed DOI PMC

Von Korff M, Radovic S, Choumane W, Stamati K, Udupa SM, Grando S, et al. Asymetric allele-specific expression in relation to developmental variation and drought stress in barley hybrids. Plant J. 2009;59: 14–26. 10.1111/j.1365-313X.2009.03848.x PubMed DOI

Song S, Li L, Yang X, Fu X, Xi M, Rocha P, et al. Expression analysis of abiotic stress-responsive genes in two rice heterotic crosses under cold, heat and drought stresses. Plant Breed. 2012;131: 276–275.

Ereful NC, Liu LY, Tsai E, Kao SM, Dixit S, Mauleon R, et al. Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs. Rice. 2016;9: 50 10.1186/s12284-016-0123-4 PubMed DOI PMC

Kong YM, Elling AA, Chen B, Deng XW. Differential expression of microRNAs in maize inbred and hybrid lines during salt and drought stress. Amer J Plant Sci. 2010;1: 69–76.

Gayacharan, Joel AJ. Epigenetic responses to drought stress in rice (Oryza sativa L.). Physiol Mol Biol Plants. 2013;19: 379–387. 10.1007/s12298-013-0176-4 PubMed DOI PMC

Mohammadi PP, Moieni A, Komatsu S. Comparative proteome analysis of drought-sensitive and drought-tolerant rapeseed roots and their hybrid F1 line under drought stress. Amino Acids. 2012;43: 2137–2152. 10.1007/s00726-012-1299-6 PubMed DOI

Fisher RA, Maurer R. Drought resistance in spring wheat cultivars. I. Grain yield responses. Austr J Agric Res. 1978;29: 897–917.

Rosielle AA, Hamblin J. Theoretical aspects of selection for yield in stress and non-stress environments. Crop Sci. 1981;21: 943–946.

Strasser RJ, Srivastava A, Tsimilli-Michael M. The fluorescence transient as a tool to characterize and screen photosynthetic samples In: Yunus M, Pathre U, Mohanty P, editors. Probing photosynthesis: Mechanism, regulation and adaptation. London: Taylor and Francis; 2000. pp. 445–483.

Stirbet A, Govindjee. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B: Biol. 2011;104: 236–257. PubMed

Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee, et al. Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta. 2010;1797:1428–1438. 10.1016/j.bbabio.2010.02.002 PubMed DOI

Bartoš J, Berková E, Šetlík I. A versatile chamber for gas exchange measurements in suspensions of algae and chloroplasts. Photosynthetica. 1975;9: 395–406.

Premachandra GS, Saneoka H, Fujita K, Ogata S. Cell membrane stability and leaf water relations as affected by nitrogen nutrition under water stress in maize. Soil Sci Plant Nutr. 1990;36: 653–659.

Benešová M, Holá D, Fischer L, Jedelský PL, Hnilička F, Wilhelmová N, et al. The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PloS ONE. 2012;7: e38017 10.1371/journal.pone.0038017 PubMed DOI PMC

Nakano Y, Asada K. Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 1981;22: 867–880.

Smith IK, Vierheller TL, Thorne CA. Assay of glutathione-reductase in crude tissue-homogenates using 5,5'-dithiobis(2-nitrobenzoic acid). Anal Biochem. 1988;175: 408–413. PubMed

Ukeda H, Maeda S, Ishii T, Sawamura M. Spectrophotometric assay for superoxide dismutase based on tetrazolium salt 3'-{1-[(phenylamino)-carbonyl]-3,4-tetrazolium}-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate reduction by xanthine-xanthine oxidase. Anal Biochem. 1997;251: 206–209. 10.1006/abio.1997.2273 PubMed DOI

Thomas DJ, Avenson TJ, Thomas JB, Herbert SK. A cyanobacterium lacking iron superoxide dismutase is sensitized to oxidative stress induced with methyl viologen but is not sensitized to oxidative stress induced with norflurazon. Plant Physiol. 1998;116: 1593–1602. PubMed PMC

Bradford MM. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem. 1976;72: 248–254. PubMed

Masuda R, Hayakawa A, Kakiuchi N, Iwamoto M. HPLC determination of total ascorbic acid in fruits and vegetables. Rep Nat Food Res Inst. 1988;52: 30–35.

Procházková D, Haisel D, Wilhelmová N. Antioxidant protection during ageing and senescence in chloroplasts of tobacco with modulated life-span. Cell Biochem Function. 2008;26: 582–590. PubMed

Kranner I. Determination of glutathione, glutathione disulphide and two related enzymes, glutathione reductase and glucose-6-phosphate dehydrogenase, in fungal and plant cells In: Varma A, editor. Mycorrhizal Manual. Berlin: Springer Verlag; 1998. pp. 227–241.

Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39: 205–207.

Tardieu F. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J Exp Bot. 2012;63: 25–31. 10.1093/jxb/err269 PubMed DOI

Jamaux I, Steinmetz A, Belhassen E. Looking for molecular and physiological markers of osmotic adjustment in sunflower. New Phytol. 1997;137: 117–127.

Chen X, Mon D, Xasir TA, Hu YG. Evaluation of 14 morphological, yield-related and physiological traits as indicators of drought tolerance in Chinese winter bread wheat revealed by analysis of the membership function value of drought tolerance (MFVD). Field Crop Res. 2012;137: 195–201.

Ryan CA, Dodd IC, Rothwell SA, Jones R, Tardieu F, Draye X, et al. Gravimetric phenotyping of whole plant transpiration responses to atmospheric vapour presure deficit identifies genotypic variation in water use efficiency. Plant Sci. 2016;251: 101–109. 10.1016/j.plantsci.2016.05.018 PubMed DOI

Shikanai T. Cyclic electron transport around Photosystem I: genetic approaches. Annu Rev Plant Biol. 2007;58: 199–217. 10.1146/annurev.arplant.58.091406.110525 PubMed DOI

Gonzáles RM, Iusem ND. Twenty years of research on Asr (ABA-stress-ripening) genes and proteins. Planta. 2014;239: 941–949. 10.1007/s00425-014-2039-9 PubMed DOI

Virlouvet L, Jacquemot MP, Gerentes D, Corti H, Bouton S, Gilard F, et al. The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol. 2011;157: 917–936. 10.1104/pp.111.176818 PubMed DOI PMC

Jeanneau M, Gerentes D, Foueillassar X, Zivy M, Vidal J, Toppan A, et al. Improvement of drought tolerance in maize: towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC. Biochimie. 2002;84: 1127–1135. PubMed

Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M. Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol. 2012;35: 1011–1019. PubMed PMC

Kolarovič L, Valentovič P, Luxová M, Gašparíková O. Changes in antioxidants and cell damage in heterotrophic maize seedlings differing in drought sensitivity after exposure to short-term osmotic stress. Plant Growth Regul. 2009;59: 21–26.

Chugh V, Kaur N, Gupta AK. Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Ind J Biochem Biophys. 2011;48: 47–53. PubMed

Sairam RK, Saxena DC. Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. J Agron Crop Sci. 2000;184: 55–61.

Secenji M, Hideg E, Bebes A, Gyorgyey J. Transcriptional differences in gene families of the ascorbate-glutathione cycle in wheat during mild water deficit. Plant Cell Rep. 2010;29: 37–50. 10.1007/s00299-009-0796-x PubMed DOI

Singh S, Gupta AK, Kaur N. Differential responses of antioxidative defence system to long-term field drought in wheat (Triticum aestivum L.) genotypes differing in drought tolerance. J Agron Crop Sci. 2012;198: 185–195.

Guo Z Ou W, Lu S, Zhong Q. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem. 2006;44: 828–836. 10.1016/j.plaphy.2006.10.024 PubMed DOI

D'Arcy-Lameta A, Ferrari-Iliou R, Contour-Ansel D, Pham-Thi AT, Zuily-Fodil Y. Isolation and characterization of four ascorbate peroxidase cDNAs responsive to water deficit in cowpea leaves. Ann Bot. 2006;97: 133–140. 10.1093/aob/mcj010 PubMed DOI PMC

Foyer CH, Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 2011;155:2–18. 10.1104/pp.110.167569 PubMed DOI PMC

Gallie DR. L-Ascorbic acid: A multifunctional molecule supporting plant growth and development. Scientifica. 2013;2013: Article ID 795964 10.1155/2013/795964 PubMed DOI PMC

Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, et al. Glutathione in plants: an integrated overview. Plant Cell Environ. 2012;35: 454–484. 10.1111/j.1365-3040.2011.02400.x PubMed DOI

Acar O, Türkan I, Özdemir F. Superoxide dismutase and peroxidase activities in drought sensitive and resistant barley (Hordeum vulgare L.) varieties. Acta Physiol Plant. 2001;23: 351–356.

Huseynova IM. Photosynthetic characteristics and enzymatic antioxidant capacity of leaves from wheat cultivars exposed to drought. Biochim Biophys Acta—Bioenergetics. 2012;1817: 1516–1523. PubMed

Minagawa J. State transitions—the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta—Bioenergetics. 2011;1807: 897–905. PubMed

Mazor Y, Borovikova A, Nelson N. The structure of plant photosystem I super-complex at 2.8 Å resolution. eLife. 2015;4: e07433 10.7554/eLife.07433 PubMed DOI PMC

Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance of crop plants. Plant Physiol Biochem. 2010;48: 909–930. 10.1016/j.plaphy.2010.08.016 PubMed DOI

Das K, Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. 2014;2: 53.

Vikram P, Swamy BPM, Dixit S, Singh R, Singh BP, Miro B et al. Drought susceptibility of modern rice varieties: an effect of linkage of drought tolerance with undesirable traits. Sci Rep. 2015;5: 14799 10.1038/srep14799 PubMed DOI PMC

Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot. 2015;115: 433–447. 10.1093/aob/mcu239 PubMed DOI PMC

Verbruggen N, Hermans C. Proline accumulation in plants: a review. Amino Acids. 2008;35: 753–759. 10.1007/s00726-008-0061-6 PubMed DOI

Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K. Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav. 2011;6: 1503–1509. 10.4161/psb.6.10.17088 PubMed DOI PMC

Graether SP, Boddington KF. Disorder and function: a review of the dehydrin protein family. Front Plant Sci. 2014;5: 576 10.3389/fpls.2014.00576 PubMed DOI PMC

Zhao Y, Du H, Wang Z, Huang B. Identification of proteins associated with water-deficit tolerance in C4 perennial grass species, Cynodon dactylon×Cynodon transvaalensis and Cynodon dactylon. Physiol Plant. 2011;141: 40–55. 10.1111/j.1399-3054.2010.01419.x PubMed DOI

Sun W, Van Montagu M, Verbruggen N. Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta—Gene Structure Expression. 2002;1577: 1–9. PubMed

Xu C, Huang B. Comparative analysis of drought responsive proteins in Kentucky bluegrass cultivars contrasting in drought tolerance. Crop Sci. 2010;50: 2543–2552.

Zadražnik T, Hollung K, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J. Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteomics. 2013;78: 254–272. 10.1016/j.jprot.2012.09.021 PubMed DOI

Hao P, Zhu J, Gu A, Lv D, Ge P, Chen G, et al. An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery. Proteomics. 2015;15: 1544–1563. 10.1002/pmic.201400179 PubMed DOI

Cheng Z, Dong K, Ge P, Bian Y, Dong L, Deng X, et al. Identification of leaf proteins differentially accumulated between wheat cultivars distinct in their levels of drought tolerance. PloS One. 2015;10: e0125302 10.1371/journal.pone.0125302 PubMed DOI PMC

Wang N, Zhao J, He X, Sun H, Zhang G, Wu F. Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. BMC Genomics. 2015;16: 432 10.1186/s12864-015-1657-3 PubMed DOI PMC

Zhou S, Li M, Guan Q, Liu F, Zhang S, Chen W, et al. Physiological and proteome analysis suggest critical roles for the photosynthetic system for high water-use efficiency under drought stress in Malus. Plant Sci. 2015;236: 44–60. 10.1016/j.plantsci.2015.03.017 PubMed DOI

Katam R, Sakata K, Suravajhala P, Pechan T, Kambiranda DM, Naik KS, et al. Comparative leaf proteomics of drought-tolerant and-susceptible peanut in response to water stress. J Proteomics. 2016;143: 209–226. 10.1016/j.jprot.2016.05.031 PubMed DOI

Shi H, Ye T, Chan Z. Comparative proteomic responses of two bermudagrass (Cynodon dactylon (L). Pers.) varieties contrasting in drought stress resistance. Plant Physiol Biochem. 2014;82: 218–228. 10.1016/j.plaphy.2014.06.006 PubMed DOI

Chmielewska K, Rodziewicz P, Swarcewicz B, Sawikowska A, Krajewski P, Marczak Ł, et al. Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Front Plant Sci. 2016;7: 1108 10.3389/fpls.2016.01108 PubMed DOI PMC

Cheng L, Wang Y, He Q, Li H, Zhang X, Zhang F. Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration. BMC Plant Biol. 2016;16: 188 10.1186/s12870-016-0871-8 PubMed DOI PMC

Ashoub A, Beckhaus T, Berberich T, Karas M, Brüggeman W. Comparative analysis of barley leaf proteome as affected by drought stress. Planta. 2013;237: 771–781. 10.1007/s00425-012-1798-4 PubMed DOI

Li X, Yang Y, Yang S, Sun X, Yin X, Zhao Y, et al. Comparative proteomics analyses of intraspecific differences in the response of Stipa purpurea to drought. Plant Diversity. 2016;38: 101–117. PubMed PMC

Bergantino E, Brunetta A, Touloupakis E, Segalla A, Szabò I, Giacometti GM. Role of the PSII-H subunit in photoprotection: novel aspects of D1 turnover in Synechocystis 6803. J Biol Chem. 2003;278: 41820–41829. 10.1074/jbc.M303096200 PubMed DOI

Shi LX, Schröder WP. The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim Biophys Acta—Bioenergetics. 2004;1608: 75–96. PubMed

Xu C, Huang B. Differential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars differing in stress tolerance. J Plant Physiol. 2010;167: 1477–1485. 10.1016/j.jplph.2010.05.006 PubMed DOI

Ford KL, Cassin A, Bacic A. Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front Plant Sci. 2011;2: 44 10.3389/fpls.2011.00044 PubMed DOI PMC

Khueychai S, Jangpromma N, Daduang S, Jaisil P, Lomthaisong K, Dhiravisit A, et al. Comparative proteomic analysis of leaves, leaf sheaths, and roots of drought-contrasting sugarcane cultivars in response to drought stress. Acta Physiol Plant. 2015;37: 88.

Riccardi F, Gazeau P, Jacquemot MP, Vincent D, Zivy M. Deciphering genetic variations of proteome responses to water deficit in maize leaves. Plant Physiol Biochem. 2004;42: 1003–1011. 10.1016/j.plaphy.2004.09.009 PubMed DOI

Kolenc Z, Vodnik D, Mandelc S, Javornik B, Kastelec D, Čerenak A. Hop (Humulus lupulus L.) response mechanisms in drought stress: Proteomic analysis with physiology. Plant Physiol Biochem. 2016;105: 67–78. 10.1016/j.plaphy.2016.03.026 PubMed DOI

Castillejo M, Maldonado AM., Ogueta S, Jorrín JV. Proteomic analysis of responses to drought stress in sunflower (Helianthus annuus) leaves by 2DE gel electrophoresis and mass spectrometry. Open Proteomics J. 2008;1: 59–71.

Faghani E, Gharechahi J, Komatsu S, Mirzaei M, Khavarinejad RA, Najafi F, et al. Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. J Proteomics. 2015;114: 1–15. 10.1016/j.jprot.2014.10.018 PubMed DOI

Kottapalli KR, Rakwal R, Shibato J, Burow G, Tissue D, Burke J, et al. Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes. Plant Cell Environ. 2009;32: 380–407. 10.1111/j.1365-3040.2009.01933.x PubMed DOI

Ji K, Wang Y, Sun W, Lou Q, Mei H, Shen S, et al. Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. J Plant Physiol. 2012;169: 336–344. 10.1016/j.jplph.2011.10.010 PubMed DOI

Bedon F, Villar E, Vincent D, Dupuy JW, Lomenech AM, Mabialangoma A, et al. Proteomic plasticity of two Eucalyptus genotypes under contrasted water regimes in the field. Plant Cell Environ. 2012;35: 790–805. 10.1111/j.1365-3040.2011.02452.x PubMed DOI

Jangpromma N, Kitthaisong S, Lomthaisong K, Daduang S, Jaisil P, Thammasirirak S. A proteomics analysis of drought stress-responsive proteins as biomarker for drought-tolerant sugarcane cultivars. Amer J Biochem Biotechnol. 2010;6: 89–102.

Marri L, Thieulin-Pardo G, Lebrun R, Puppo R, Zaffagnini M, Trost P, et al. CP12-mediated protection of Calvin–Benson cycle enzymes from oxidative stress. Biochimie. 2014;97: 228–237. 10.1016/j.biochi.2013.10.018 PubMed DOI

Gontero B, Maberly SC. An intrinsically disordered protein, CP12: jack of all trades and master of the Calvin cycle. Biochem Soc Trans. 2012;40: 995–999. 10.1042/BST20120097 PubMed DOI

Jedmowski C, Ashoub A, Beckhaus T, Berberich T, Karas M, Brüggemann W. Comparative analysis of Sorghum bicolor proteome in response to drought stress and following recovery. Int J Proteomics. 2014;2014: 395905 10.1155/2014/395905 PubMed DOI PMC

Doubnerová Hýsková V, Miedzińska L, Dobrá J, Vaňková R, Ryšlavá H. Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. J Plant Physiol. 2014;171: 19–25. 10.1016/j.jplph.2013.10.017 PubMed DOI

Hýsková V, Ryšlavá H. Unusual properties and functions of plant pyruvate, orthophosphate dikinase. Biochem Anal Biochem. 2016;5: 1.

Shen JR. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol. 2015;66: 23–48. 10.1146/annurev-arplant-050312-120129 PubMed DOI

Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008;13: 178–182. 10.1016/j.tplants.2008.01.005 PubMed DOI

Shinopoulos KE, Brudvig GW. Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta—Bioenergetics. 2012;1817: 66–75. PubMed

Barber J, Morris E, Büchel C. Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta—Bioenergetics. 2000;1459: 239–247. PubMed

Roose JL, Frankel LK, Mummadisetti MP, Bricker TM. The extrinsic proteins of photosystem II: update. Planta. 2016;243: 889–908. 10.1007/s00425-015-2462-6 PubMed DOI

Kakiuchi S, Uno C, Ido K, Nishimura T, Noguchi T, Ifuku K, et al. The PsbQ protein stabilizes the functional binding of the PsbP protein to photosystem II in higher plants. Biochim Biophys Acta—Bioenergetics. 2012;1817: 1346–1351. PubMed

Allahverdiyeva Y, Suorsa M, Rossi F, Pavesi A, Kater MM, Antonacci A, et al. Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms. Plant J. 2013;75: 671–684. 10.1111/tpj.12230 PubMed DOI

Ort DR, Merchant SS, Alric J, Barkan A, Blankenship R, Bock R, et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA. 2015;112: 8529–8536. 10.1073/pnas.1424031112 PubMed DOI PMC

White CN, Rivin CJ. Sequence and regulation of a late embryogenesis abundant group 3 protein of maize. Plant Physiol. 1995;108: 1337 PubMed PMC

Ried JL, Walker-Simmons MK. Group 3 late embryogenesis abundant proteins in desiccation-tolerant seedlings of wheat (Triticum aestivum L.). Plant Physiol. 1993;102: 125–131. PubMed PMC

Zhao P, Liu F, Zheng G, Liu H. Group 3 late embryogenesis abundant protein in Arabidopsis: structure, regulation, and function. Acta Physiol Plant. 2011;33: 1063–1073.

Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, et al. ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol. 2013;54: 944–959. 10.1093/pcp/pct047 PubMed DOI

Liu Y, Liang J, Sun L, Yang X, Li D. Group 3 LEA protein, ZmLEA3, is involved in protection from low temperature stress. Front Plant Sci. 2016;7: 1011 10.3389/fpls.2016.01011 PubMed DOI PMC

Vaseva I, Sabotič J, Šustar-Vozlič J, Meglič V, Kidrič M, Demirevska K, et al. The response of plants to drought stress: the role of dehydrins, chaperones, proteases and protease inhibitors in maintaining cellular protein function In: Neves DF, Sanz JD, editors. Droughts: New Research. New York: Nova Science Publishers; 2012. pp. 1–45.

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