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Review Articles

Drought stress-induced physiological mechanisms, signaling pathways and molecular response of chloroplasts in common vegetable crops

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Pages 669-691 | Received 07 Jan 2021, Accepted 07 Jan 2021, Published online: 01 Feb 2021

References

  • Singh D, Laxmi A. Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci. 2015;6:895.
  • Singh B, Bohra A, Mishra S, et al. Embracing new-generation ‘omics’ tools to improve drought tolerance in cereal and foodlegume crops. Biologia Plant. 2015;59:413–428.
  • Jogaiah S, Govind SR, Tran LSP. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit Rev Biotechnol. 2013;33:23–29.
  • Boyer JS. Plant productivity and environment. Science. 1982;218:443–448.
  • Cramer GR, Urano K, Delrot S, et al. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 2011;11:163–176.
  • Zhang D, Tong J, He X, et al. A novel soybean intrinsic protein gene, GmTIP2;3, Involved in responding to osmotic stress. Front Plant Sci. 2015;6:1237.
  • Tester M, Langridge P. Breeding technologies to increase crop production in a changing world. Science. 2010;327:818–822.
  • Pervez MA, Ayub CM, Khan HA, et al. Effect of drought stress on growth, yield and seed quality of tomato (Lycopersicon esculentum L.) Pak. J Agri Sci. 2009;46:174–178.
  • Iqbal N, Hussain S, Raza MA, et al. Drought tolerance of soybean (Glycine max L. Merr.) by improved photosynthetic characteristics and an efficient antioxidant enzyme activities under a split-root system. Front Physiol. 2019;10:786.
  • Tardieu F, Simonneau T, Muller B. The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu Rev Plant Biol. 2018;69:733–759.
  • Demidchik V. ROS-activated ion channels in plants: biophysical characteristics, physiological functions and molecular nature. Int J Mol Sci. 2018;19:1263.
  • Ernst L, Goodger JQ, Alvarez S, et al. Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. J Exp Bot. 2010;61:3395–3405.
  • Malcheska F, Ahmad A, Batool S, et al. Drought-enhanced xylem sap sulfate closes stomata by affecting ALMT12 and guard cell ABA synthesis. Plant Physiol. 2017;174:798–814.
  • Batool S, Uslu VV, Rajab H, et al. Sulfate is incorporated into cysteine to trigger ABA production and stomatal closure. Plant Cell. 2018;30:2973–2987.
  • Manickavelu A, Nadarajan N, Ganesh SK, et al. Drought tolerance in rice: morphological and molecular genetic consideration. Plant Growth Regul. 2006;50:121–138.
  • Sun X, Sun M, Luo X, et al. A Glycine soja ABA-responsive receptor-like cytoplasmic kinase, GsRLCK, positively controls plant tolerance to salt and drought stresses . Planta. 2013;237:1527–1545.
  • Wahid A, Shabbir A. Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycine betaine. Plant Growth Regul. 2005;46:133–141.
  • Munemasa S, Hauser F, Park J, et al. Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol. 2015;28:154–162.
  • Geiger D, Maierhofer T, Al-Rasheid KAS, et al. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal. 2011;4:ra32.
  • Bartlett MK, Klein T, Jansen S, et al. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci USA. 2016;113:13098–13103.
  • Leonhardt N, Kwak JM, Robert N, et al. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell. 2004;16:596–615.
  • Pitman MG, Wellfare D. Inhibition of ion-transport in excised barley roots by abscisic-acid – relation to water permeability of roots. J Exp Bot. 1978;29:1125–1138.
  • Ma Y, Cao J, He J, et al. Molecular mechanism for the regulation of aba homeostasis during plant development and stress responses. IJMS. 2018;19:3643.
  • Shabala SN, Lew RR. Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol. 2002;129:290–299.
  • Scharwies JD, Dinneny JR. Water transport, perception, and response in plants. J Plant Res. 2019;132:311–324.
  • Marschner P. Marschner’s mineral nutrition of higher plants. 3rd ed. San Diego (CA): Academic Press; 2012.
  • Shabala S. Signalling by potassium: another second messenger to add to the list? J Exp Bot. 2017;68:4003–4007.
  • Chen G, Liu C, Gao Z, et al. OsHAK1, a High-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci. 2017;8:1885.
  • Franco-Navarro JD, Rosales MA, Álvarez R, et al. Chloride as a macronutrient increases water-use efficiency by anatomically driven reduced stomatal conductance and increased mesophyll diffusion to CO2. Plant J. 2019;99:815–831.
  • Maron LG. From foe to friend: the role of chloride as a beneficial macronutrient. Plant J. 2019;99:813–814.
  • Franco-Navarro JD, Brumos J, Rosales MA, et al. Chloride regulates leaf cell size and water relations in tobacco plants. J Exp Bot. 2016;67:873–891.
  • Colmenero-Flores JM, Franco-Navarro JD, Cubero-Font P, et al. Chloride as a beneficial macronutrient in higher plants: new roles and regulation. IJMS. 2019;20:4686.
  • Tariq A, Pan t, Olatunji OA, et al. Impact of phosphorus application on drought resistant responses of Eucalyptus grandis seedlings. Physiol Plant. 2019;166:894–908.
  • Mahpara S, Shahnawaz M, Rehman K, et al. Nitrogen fertilization induced drought tolerance in sunflower: a review. PAB. 2019;8:1675–1683.
  • Garcia-Sanchez F, Simon-Grao S, Perez-Perez JG, et al. Methods used for the improvement of crop productivity under water stress. In: Ahmad P, editor. Water stress and crop plant: a sustainable approach. Vol 2. West Sussex (UK): John Wiley & Sons; 2016. p. 484–505.
  • Jin J, Zhang H, Kong L, et al. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 2014;42:D1182–D1187.
  • Alqudah AM, Schnurbusch T. Barley leaf area and leaf growth rates are maximized during the pre-anthesis phase. Agronomy. 2015;5:107–129.
  • Quan W, Liu X, Wang H, et al. Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa varieties. Front Plant Sci. 2015;6:1256.
  • Georgii E, Jin M, Zhao J, et al. Relationships between drought, heat and air humidity responses revealed by transcriptome-metabolome co-analysis. BMC Plant Biol. 2017;17:120–120.
  • Petrov P, Petrova A, Dimitrov I, et al. Relationships between leaf morpho-anatomy, water status and cell membrane stability in leaves of wheat seedlings subjected to severe soil drought. J Agro Crop Sci. 2018;204:219–227.
  • Potopová V, Boroneanţ C, Boincean B, et al. Impact of agricultural drought on main crop yields in the Republic of Moldova. Int J Climatol. 2016;36:2063–2082.
  • Rollins JA, Habte E, Templer SE, et al. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J Exp Bot. 2013;64:3201–3212.
  • Anjum SA, Xie X, Wang L. Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agri Res. 2011;6:2026–2032.
  • Siddiqui MH, Al-Khaishany MY, Qutami MAA, et al. Morphological and physiological characterization of different genotypes of faba bean under heat stress. Saudi J Biol Sci. 2015;22:656–666.
  • Kaewsuksaeng S. Chlorophyll degradation in horticultural crops. Walailak J Sci Technol. 2011;8:9–19.
  • Ashraf M, Harris PJC. Photosynthesis under stressful environments: an overview. Photosynt. 2013;51:163–190.
  • Li L, Zhang Q, Huang D. A review of imaging techniques for plant phenotyping. Sensors (Basel). 2014;14:20078–20111.
  • Setter TL. Analysis of constituents for phenotyping drought tolerance in crop improvement. Front Physiol. 2012;3:180.
  • Honsdorf N, March TJ, Berger B, et al. High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines. PLoS One. 2014;9:e97047.
  • Porporato A, Laio F, Ridolfi L, et al. Plants in water‐controlled ecosystems: active role in hydrologic processes and response to water stress. III. Vegetation water stress. Adv Water Res. 2001;24:725–744.
  • Schwarz D, Rouphael Y, Colla G, et al. Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Scientia Hort. 2010;127:162–171.
  • Chakraborty U, Pradhan B. Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Braz J Plant Physiol. 2012;24:117–130.
  • Buchanan B, Gruissem W, Jones RL. Biochemistry and molecular biology of plants. Rockville (MD): American Society of Plant Physiologists; 2000.
  • Sun QZB, Majeran W, Friso G, et al. PPDB, the plant proteomics database at Cornell. Nucleic Acids Res. 2009;37:969–974.
  • Taylor NL, Heazlewood JL, Day DA, et al. Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics. 2005;4:1122–1133.
  • Carmo-Silva AE, Gore MA, Andrade-Sanchez P, et al. Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ Exp Bot. 2012;83:1–11.
  • Zhou Y, Lam HM, Zhang J. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot. 2007;58:1207–1217.
  • Kondrák M, Marincs F, Antal F, et al. Effects of yeast trehalose-6-phosphate synthase 1 on gene expression and carbohydrate contents of potato leaves under drought stress conditions. BMC Plant Biol. 2012;12:74.
  • Obidiegwu JE, Bryan GJ, Jones HG, et al. Coping with drought: stress and adaptive responses in potato and perspectives for improvement. Front Plant Sci. 2015;6:542.
  • Hadiarto T, Tran LP. Progress studies of drought-responsive genes in rice. Plant Cell Rep. 2011;30:297–310.
  • Srivalli B, Sharma G, Khanna-Chopra R. Antioxidative defense system in an upland rice cultivar subjected to increasing intensity of water stress followed by recovery. Physiol Plant. 2003;119:503–512.
  • Hussain S, Khan F, Cao W, et al. Seed priming alters the production and detoxification of reactive oxygen intermediates in rice seedlings grown under sub-optimal temperature and nutrient supply. Front Plant Sci. 2016;7:439.
  • Kosova K, Vitamvas P, Prasil IT, et al. Plant proteome changes under abiotic stress-contribution of proteomic studies to understanding plant stress response. J of Proteomics. 2011;74:1301–1322.
  • Perlikowski D, Kosmala A, Rapacz M, et al. Influence of short-term drought conditions and subsequent re-watering on the physiology and proteome of Lolium multiflorum/Festuca arundinacea introgression forms, with contrasting levels of tolerance to long-term drought. Plant Biol (Stuttg). 2014;16:385–394.
  • Wang H, Wang H, Shao H, et al. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci. 2016;7:67.
  • Nouri MZ, Komatsu S. Subcellular protein overexpression to develop abiotic stress tolerant plants. Front Plant Sci. 2013;4:2.
  • Vishwakarma K, Upadhyay N, Kumar N, et al. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci. 2017;8:161.
  • Banerjee A, Roychoudhury A. Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul. 2016;79:1–17.
  • Ling H, Zeng X, Guo S. Functional insights into the late embryogenesis abundant (LEA) protein family from Dendrobium officinale (Orchidaceae) using an Escherichia coli system. Sci Rep. 2016; 6:39693.
  • Le TTT, Williams B, Mundree SG. An osmotin from the resurrection plant Tripogon loliiformis (TlOsm) confers tolerance to multiple abiotic stresses in transgenic rice. Physiol Plant. 2018;162:13–34.
  • Ohama N, Sato H, Shinozaki K, et al. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 2017;22:53–65.
  • Zhu JK. Abiotic stress signaling and responses in plants. Cell. 2016;167:313–324.
  • Bruley C, Dupierris V, Salvi D, et al. AT_CHLORO: a chloroplast protein database dedicated to sub-plastidial localization. Front Plant Sci. 2012;3:279–286.
  • Ferro M, Brugière S, Salvi D, et al. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics. 2010;9:1063–1084.
  • Rahnama A, Poustini K, Tavakkol-Afshari R, et al. Growth and stomatal responses of bread wheat genotypes in tolerance to salt stress. Int J Biol Life Sci. 2010;6:216–221.
  • Kosmala A, Perlikowski D, Pawłowicz I, et al. Changes in the chloroplast proteome following water deficit and subsequent watering in a high- and a low-drought-tolerant genotype of Festuca arundinacea. J Exp Bot. 2012;63:6161–6172.
  • Rinalducci S, Murgiano L, Zolla L. Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot. 2008;59:3781–3801.
  • Galvez-Valdivieso G, Mullineaux PM. The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant. 2010;138:430–439.
  • Saravanavel R, Ranganathan R, Anantharaman P. Effect of sodium chloride on photosynthetic pigments and photosynthetic characteristics of Avicennia officinalis seedlings. Recent Res Sci Technol. 2011;3:177–180.
  • Leister D. Chloroplast research in the genomic age. Trends Genet. 2003;19:47–56.
  • Heazlewood JL, Verboom RE, Tonti-Filippini J, et al. SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res. 2007;35:213–218.
  • Kleffmann T, Hirsch-Hoffmann M, Gruissem W, et al. Plprot: a comprehensive proteome database for different plastid types. Plant Cell Physiol. 2006;47:432–436.
  • Sandra KT, Castleden I, Cornelia M, et al. SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 2012;41:1185–1191.
  • Joshi HJ, Hirsch-Hoffmann M, Baerenfaller K, et al. MASCP Gator: an aggregation portal for the visualization of Arabidopsis proteomics data. Plant Physiol. 2011;155:259–270.
  • Agrawal GK, Bourguignon J, Rolland N, et al. Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom Rev. 2011;30:772–853.
  • van Wijk KJ, Baginsky S. Plastid proteomics in higher plants: current state and future goals. Plant Physiol. 2011;155:1578–1588.
  • Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–399.
  • Mittler R, Vanderauwera S, Gollery M, et al. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498.
  • Mittler R. Oxidative stress, antioxidant and stress tolerance. Trends Plant Sci. 2002;7:405–410.
  • Møller IM, Sweetlove LJ. ROS signalling-specificity is required. Trends Plant Sci. 2010;15:370–374.
  • Karuppanapandian T, Moon JC, Kim C, et al. Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci. 2011;5:709–725.
  • Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006;141:391–396.
  • Lee KP, Kim C, Landgraf F, et al. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA. 2007;104:10270–10275.
  • Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Biol. 2007;58:459–481.
  • Triantaphylidès C, Krischke M, Hoeberichts FA, et al. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 2008;148:960–968.
  • Navrot N, Rouhier N, Gelhaye E, et al. Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant. 2007;129:185–195.
  • Noctor G, De Paepe R, Foyer CH. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 2007;12:125–134.
  • Rasmusson AG, Geisler DA, Møller IM. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion. 2008;8:47–60.
  • Pastore D, Trono D, Laus MN, et al. Possible plant mitochondria involvement in cell adaptation to drought stress a case study: durum wheat mitochondria. J Exp Bot. 2007;58:195–210.
  • Luis A, Sandalio LM, Corpas FJ, et al. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 2006;141:330–335.
  • Palma JM, Corpas FJ, del Río LA. Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics. 2009;9:2301–2312.
  • Noctor G, Veljovic-Jovanovic S, Driscoll S, et al. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann of Bot. 2002;89:841–850.
  • Scandalios JG. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res. 2005;38:995–1014.
  • Gratão PL, Polle A, Lea PJ, et al. Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol. 2005;32:481–494.
  • Smirnoff N. Ascorbic acid: metabolism and functions of a multifaceted molecule. Current Opinions in Plant Biol. 2000;3:229–235.
  • Sharma P, Jha AB, Dubey RS, et al. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J of Bot. 2012;2012:1–26.
  • Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:601–639.
  • Scandalios JG. The rise of ROS. Trends Biochem Sci. 2002;27:483–486.
  • Pareek A, Sopory SK, Bohnert HK, et al. Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Dordrecht (the Netherlands): Springer; 2010.
  • Joshi R, Singh B, Bohra A, et al. Salt stress signalling pathways: specificity and crosstalk. In: Wani SH, Hossain MA, editors. Managing salinity tolerance in plants: molecular and genomic perspectives. Boca Raton (FL): CRC Press; 2016. p. 51–78.
  • Todaka D, Nakashima K, Shinozaki K, et al. Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice (N Y). 2012;5:6.
  • Ray S, Dansana PK, Bhaskar A, et al. Emerging trends in functional genomics for stress tolerance in crop plants. In: Hirt H, editor. Plant stress biology: from genomics to systems biology. Weinheim (Germany): Wiley-VCH; 2010. p. 37–63.
  • Sanchez DH, Pieckenstain FL, Szymanski J, et al. Comparative functional genomics of salt stress in related model and cultivated plants identifies and overcomes limitations to translational genomics. PLoS One. 2011;6:e17094.
  • Roy SJ, Negrão S, Tester M. Salt resistant crop plants. Curr Opin Biotechnol. 2014; 26:115–124.
  • Oono Y, Seki M, Satou M, et al. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics. 2006;6:212–234.
  • Mantri NL, Ford R, Coram TE, et al. Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics. 2007;8:303.
  • Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006;57:781–803.
  • Kuromori T, Sugimoto E, Shinozaki K. Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiol. 2014;164:1587–1592.
  • Ahmad P, Rasool S, Gul A, et al. Jasmonates: multifunctional roles in stress tolerance. Front in Plant Sci. 2016;7:813.
  • Yu XX, Zhang W, Zhang Y, et al. The roles of methyl jasmonate to stress in plants. Funct Plant Biol. 2019;46:197–212.
  • Savchenko TV, Rolletschek H, Dehesh K. Jasmonates-mediated rewiring of central metabolism regulates adaptive responses. Plant Cell Physiol. 2019;60:2613–2620.
  • Kanagendran A, Chatterjee P, Liu B, et al. Foliage inoculation by Burkholderia vietnamiensis CBMB40 antagonizes methyl jasmonate-mediated stress in Eucalyptus grandis. J Plant Physiol. 2019;242:153032.
  • Jiang YF, Ye JY, Li S, et al. Methyl jasmonate-induced emission of biogenic volatiles is biphasic in cucumber: a high-resolution analysis of dose dependence. J Exp Bot. 2017;68:4679–4694.
  • Shi J, Ma CY, Qi DD, et al. Transcriptional responses and flavor volatiles biosynthesis in methyl jasmonate-treated tea leaves. BMC Plant Biol. 2015;15:1–10.
  • Sadeghipour O. Amelioration of salinity tolerance in cowpea plants by seed treatment with methyl jasmonate. Legume Res. 2017;40:1100–1106.
  • Ahmadi FI, Karimi K, Struik PC. Effect of exogenous application ofmethyljasmonate on physiological and biochemical characteristics of Brassica napus L. cv. Talaye under salinity stress. South Afr J Bot. 2018;115:5–11.
  • Rohwer CL, Erwin JE. Horticultural applications of jasmonates: a review. J Hortic Sci Biotech. 2008;83:283–304.
  • Riemann M, Dhakarey R, Hazman M, et al. Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci. 2015;1:6.
  • Chini A, Fonseca S, Fernández G, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 2007;448:666–671.
  • Park JH, Saier MH. Phylogenetic characterization of the MIP family of transmembrane channel proteins. J Membr Biol. 1996;153:171–180.
  • Kozono D, Ding X, Iwasaki I, et al. Functional expression and characterization of an archaeal aquaporin. AqpM from Methanothermobacter marburgensis. J Biol Chem. 2003;278:10649–10656.
  • Kaldenhoff R, Fischer M. Functional aquaporin diversity in plants. Biochim Biophys Acta. 2006;1758:1134–1141.
  • Lian HL, Yu X, Lane D, et al. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res. 2006;16:651–660.
  • Guo L, Wang ZY, Lin H, et al. Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res. 2006;16:277–286.
  • Hachez C, Moshelion M, Zelazny E, et al. Chaumont, Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol. 2006;62:305–323.
  • Zhang Y, Wang Z, Chai T, et al. Indian mustard aquaporin improves drought and heavy-metal resistance in tobacco. Mol Biotechnol. 2008;40:280–292.
  • Cui XH, Hao FS, Chen H, et al. Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance. J Plant Res. 2008;121:207–214.
  • Pou A, Medrano H, Flexas J, et al. A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant Cell Environ. 2013;36:828–843.
  • Heinen RB, Bienert GP, Cohen D, et al. Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays. Plant Mol Biol. 2014;86:335–350.
  • Ariani A, Gepts P. Genome-wide identification and characterization of aquaporin gene family in common bean (Phaseolus vulgaris L.). Mol Genet Genomics. 2015;290:1771–1785.
  • Shatil-Cohen A, Attia Z, Moshelion M. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J. 2011;67:72–80.
  • Pantin F, Monnet F, Jannaud D, et al. The dual effect of abscisic acid on stomata. New Phytol. 2013;197:65–72.
  • Sade N, Shatil-Cohen A, Moshelion M. Bundle-sheath aquaporins play a role in controlling Arabidopsis leaf hydraulic conductivity. Plant Signal Behav. 2015;10:e1017177.
  • Machado JL, Tyree MT. Patterns of hydraulic architecture and water relations of two tropical canopy trees with contrasting leaf phenologies: Ochroma pyramidale and Pseudobombax septenatum. Tree Physiol. 1994;14:219–240.
  • Meinzer FC. Co-ordination of vapour and liquid phase water transport properties in plants. Plant Cell Environ. 2002;25:265–274.
  • De Smet I, Zhang H. Abscisic acid in root growth and development. In: Eshel A, Beeckman T, editors. Plant roots: the hidden half. Vol. 16. Boca Raton (FL): CRC Press; 2013. p. 1–13.
  • Grondin A, Rodrigues O, Verdoucq L, etal. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell. 2015;27:1945–1954.
  • Heinen RB, Ye Q, Chaumont F. Role of aquaporins in leaf physiology. J Exp Bot. 2009; 60:2971–2985.
  • Tsuchihira A, Hanba YT, Kato N, et al. Effect of overexpression of radish plasma membrane aquaporins on water-use efficiency, photosynthesis and growth of Eucalyptus trees. Tree Physiol. 2010;30:417–430.
  • Jarzyniak KM, Jasiński M. Membrane transporters and drought resistance – a complex issue. Plant Traffic and Transport. 2014;5:687.
  • Moshelion M, Halperin O, Wallach R, et al. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant Cell Environ. 2015;38:1785–1793.
  • Ding L, Gao L, Liu W, et al. Aquaporin plays an important role in mediating chloroplastic CO2 concentration under high-N supply in rice (Oryza sativa) plants. Physiol Plant. 2016;156:215–226.
  • Laur J, Hacke UG. Transpirational demand affects aquaporin expression in poplar roots. J Exp Bot. 2013;64:2283–2293.
  • Dang NX, Popova AV, Hundertmark M, et al. Functional characterization of selected LEA proteins from Arabidopsis thaliana in yeast and in vitro. Planta. 2014;240:325–336.
  • Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:571–599.
  • Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot. 2007;58:221–227.
  • Ismail AM, Hall AE, Close TJ. Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol. 1999;120:237–244.
  • Magwanga RO, Lu P, Kirungu JN, et al. Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet. 2018;19:6.
  • Chen Y, Li C, Zhang B, et al. The role of the late embryogenesis-abundant (LEA) protein family in development and the abiotic stress response: a comprehensive expression analysis of potato (Solanum tuberosum). Genes. 2019;10:148.
  • Shih MD, Hoekstra FA, Hsing YIC. Late embryogenesis abundant proteins. Adv Bot Res. 2008;48:211–255.
  • Hand SC, Menze MA, Toner M, et al. LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol. 2011;73:115–1134.
  • Tunnacliffe A, Hincha DK, Leprince O, et al. LEA proteins: versatility of form and function. In: Lubzens E, Cerda J, Clark M, editors. Dormancy and resistance in harsh environments. Berlin (Germany): Springer; 2010. p. 91–108.
  • Kovacs D, Kalmar E, Torok Z, et al. Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol. 2008;147:381–3390.
  • Hincha DK, Thalhammer A. LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem Soc Trans. 2012;40:1000–1003.
  • Cuevas-Velazquez CL, Reyes JL, Covarrubias AA. Group 4 late embryogenesis abundant proteins as a model to study intrinsically disordered proteins in plants. Plant Signal and Behav. 2017;12:10893e–110903.
  • Swindell WR, Huebner M, Weber AP. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics. 2007;8:125.
  • Al-Whaibi MH. Plant heat-shock proteins: a mini review. JofKing Saud Univ Sci. 2011;23:139–150.
  • Xu Y, Zhan C, Huang B. Heat shock proteins in association with heat tolerance in grasses. Int J Proteomics. 2011;2011:529648.
  • Breiman A. Plant Hsp90 and its co-chaperones. Curr Protein Pept Sci. 2014;15:232–244.
  • Pandey A, Rajamani U, Verma J, et al. Identification of extracellular matrix proteins of rice (Oryza sativa L.) involved in dehydration-responsive network: a proteomic approach. J Proteome Res. 2010;9:3443–3464.
  • Bhushan D, Jaiswal DK, Ray D, et al. Dehydration-responsive reversible and irreversible changes in the extracellular matrix: comparative proteomics of chickpea genotypes with contrasting tolerance. J Proteome Res. 2011;10:2027–2046.
  • Pearl LH, Prodromou C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem. 2006; 75:271–294.
  • Schopf FH, Biebl MM, Buchner J. The HSP90 chaperone machinery. Nat Rev Mol Cell Biol. 2017;18:345–360.
  • Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol. 2010;11:515–528.
  • Hahn A, Bublak D, Schleiff E, et al. Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell. 2011;23:741–755.
  • Meiri D, Breiman A. Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J. 2009;59:387–399.
  • Moshe A, Gorovits R, Liu Y, et al. Tomato plant cell death induced by inhibition of HSP90 is alleviated by Tomato yellow leaf curl virus infection. Mol Plant Pathol. 2016;17:247–260.
  • Zhang J, Liu B, Li J, et al. Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics. 2015;16:181.
  • Pandey A, Chakraborty S, Datta A, et al. Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol Cell Proteomics. 2008;7:88–107.
  • Choudhary MK, Basu D, Datta A, et al. Dehydration-responsive nuclear proteome of rice (Oryza sativa L.) illustrates protein network, novel regulators of cellular adaptation, and evolutionary perspective. Mol Cell Proteomics. 2009;8:1579–1598.
  • Subba P, Barua P, Kumar R, et al. Phosphoproteomic dynamics of chickpea (Cicer arietinum L.) reveals shared and distinct components of dehydration response. J Proteome Res. 2013;12:5025–5047.
  • Cruz de Carvalho R, Bernardes DA Silva A, Soares R, et al. Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ. 2014;37:1499–1515.
  • Low D, Brandle K, Nover L, et al. Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta. 2000;211:575–582.
  • Chan KX, Phua SY, Crisp P, et al. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol. 2016;67:25–53.
  • Bobik K, Burch-Smith TM. Chloroplast signaling within, between and beyond cells. Front Plant Sci. 2015;6:781.
  • Bräutigam K, Dietzel L, Pfannschmidt T. Plastid-nucleus communication: anterograde and retrograde signalling in the development and function of plastids. In: Bock R, editor. Cell and molecular biology of plastids. Berlin (Germany): Springer; 2007. p. 409–455.
  • Chi W, Sun X, Zhang L. Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol. 2013;64:559–582.
  • Estavillo GM, Crisp PA, Pornsiriwong W, et al. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell. 2011;23:3992–4012.
  • Pornsiriwong W, Estavillo GM, Chan KX, et al. A chloroplast retrograde signal, 30 -phosphoadnenosine 50 -phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. eLife. 2017;6:e23361.
  • Umezawa T, Nakashima K, Miyakawa T, et al. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 2010;51:1821–1839.
  • Cutler SR, Rodriguez PL, Finkelstein RR, et al. Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol. 2010;61:651–679.
  • Köhler B, Hills A, Blatt MR. Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol. 2003;131:385–388.
  • Kwak JM, Mori IC, Pei ZM, et al. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. Embo J. 2003;22:2623–2633.
  • Chen ZH, Hills A, Lim CK, et al. Dynamic regulation of guard cell anion channels by cytosolic free Ca2+ concentration and protein phosphorylation. Plant J. 2010;61:816–825.
  • Hosy E, Vavasseur A, Mouline K, et al. The Arabidopsis outward K + channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA. 2003;100:5549–5554.
  • Gallardo K, Courty PE, Le Signor C, et al. Sulfate transporters in the plant’s response to drought and salinity: regulation and possible functions. Front Plant Sci. 2014;5:580.
  • Jezek M, Blatt MR. The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiol. 2017;174:487–519.
  • Saier MH, Yen MR, Noto K, et al. The transporter classification database: recent advances. Nucleic Acids Res. 2009;37:D274–D278.
  • Yabuta Y, Maruta T, Yoshimura K, et al. Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol. 2004;45:1586–1594.
  • Pribil M, Labs M, Leister D. Structure and dynamics of thylakoids in land plants. J Exp Bot. 2014;65:1955–1972.
  • Marmagne A, Vinauger-Douard M, Monachello D, et al. Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively. J Exp Bot. 2007;58:3385–3393.
  • Spetea C, Schoefs B. Solute transporters in plant thylakoid membranes: key players during photosynthesis and light stress. Commun Integr Biol. 2010;3:122–129.
  • Finazzi G, Petroutsos D, Tomizioli M, et al. Ions channels/transporters and chloroplast regulation. Cell Calcium. 2015;58:86–97.
  • Wang C, Yamamoto H, Narumiy F, et al. Fine-tuned regulation of the K+ /H + antiporter KEA3 is required to optimize photosynthesis during induction. Plant J. 2017;89:540–553.
  • Froehlich JE, Wilkerson CG, Ray WK, et al. Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J Proteome Res. 2003;2:413–425.
  • Redinbo MR, Yeates TO, Merchant S. Plastocyanin: Structural and functional analysis. J Bioenerg Biomembr. 1994;26:49–66.
  • Von Gromoff ED, Alawady A, Meinecke L, et al. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell. 2008;20:552–567.
  • Woodson JD, Perez-Ruiz JM, Chory J. Heme synthesis by plastid Ferrochelatase I regulates nuclear gene expression in plants. Curr Biol. 2011;21:897–903.
  • Cao MJ, Wang Z, Wirtz M, et al. SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J. 2013;73:607–616.
  • Klein M, Geisler M, Suh SJ, et al. Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J. 2004;39:219–236.
  • Mugford SG, Yoshimoto N, Reichelt M, et al. Disruption of adenosine-5'-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell. 2009;21:910–927.
  • Rossel JB, Walter PB, Hendrickson L, et al. A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ. 2006;29:269–281.
  • Wilson PB, Estavillo GM, Field KJ, et al. The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J. 2009;58:299–317.
  • Chen ZH, Wang Y, Wang JW, et al. Nitrate reductase mutation alters potassium nutrition as well as nitric oxide-mediated control of guard cell ion channels in Arabidopsis. New Phytol. 2016;209:1456–1469.
  • Cai S, Papanatsiou M, Blatt MR, et al. Speedy grass stomata: emerging molecular and evolutionary features. Mol Plant. 2017;10:912–914.
  • Kinoshita T, Doi M, Suetsugu N, et al. Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature. 2001;414:656–660.
  • Kwak JM, Murata Y, Baizabal-Aguirre VM, et al. Dominant negative guard cell K + channel mutants reduce inward-rectifying K + currents and Light-Induced stomatal opening in Arabidopsis. Plant Physiol. 2001;127:473–485.
  • White PJ, Bowen HC, Demidchik V, et al. Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochem Biophys Acta Biomembrane. 2002;1564:299–309.
  • Blatt MR. Ca2+ signalling and control of guard-cell volume in stomatal movements. Current Opinion in Plant Biol. 2000;3:196–204.
  • Kim TH, Bohmer M, Hu H, et al. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol. 2010;61:561–591.
  • Latz A, Becker D, Hekman M, et al. TPK1, a Ca(2+)-regulated Arabidopsis vacuole two-pore K(+) channel is activated by 14-3-3 proteins. Plant J. 2007;52:449–459.
  • Latz A, Mehlmer N, Zapf S, et al. Salt stress triggers phosphorylation of the Arabidopsis vacuolar K + channel TPK1 by calcium-dependent protein kinases (CDPKs). Mol Plant. 2013;6:1274–1289.
  • Geiger D, Scherzer S, Mumm P, et al. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA. 2009;106:21425–21430.
  • Zargar SM, Mahajan R, Nazir M, et al. Common bean proteomics: present status and future strategies. J Proteomics. 2017;169:239–248.
  • Zadražnik T, Moen A, Šuštar-Vozlič J. Jelka Šuštar Vozlič3.Chloroplast proteins involved in drought stress response in selected cultivars of common bean (Phaseolus vulgaris L.). 3 Biotech. 2019;9:331.
  • Lu C, Zhang J. Effects of water stress on photosystem II photochemistry and its thermo stability in wheat plants. J Exp Bot. 1999;50:1199–1206.
  • Hajheidari M, Abdollahian-Noghabi M, Askari H, et al. Proteome analysis of sugar beet leaves under drought stress. Proteomics. 2005;5:950–960.
  • Li C, Bian B, Gong T, et al. Comparative proteomic analysis of key proteins during abscisic acid-hydrogen peroxide-induced adventitious rooting in cucumber (Cucumis sativus L.) under drought stress. J Plant Physiol. 2018;229:185–194.
  • Han Q, Kang G, Guo T. Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem. 2013;63:236–244.
  • Moolna A, Bowsher CG. The physiological importance of photosynthetic ferredoxin NADP + oxidoreductase (FNR) isoforms in wheat. J Exp Bot. 2010;61:2669–2681.
  • Komenda J, Nickelsen J, Tichy M, et al. The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803 . J Biol Chem. 2008;283:22390–22399.
  • Yang H, Liu J, Wen X, et al. Molecular mechanism of photosystem I assembly in oxygenic organisms. Biochim Biophys Acta. 2015;1847:838–848.
  • Armbruster U, Labs M, Pribil M, et al. Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell. 2013;25:2661–26678.
  • Wang J, Yu Q, Xiong H, et al. Proteomic insight into the response of Arabidopsis chloroplasts to darkness. PLoS One. 2016;11:e0154235.
  • Athar HR, Ashraf M. Photosynthesis under drought stress. In: Pessarakli M, editor. Handbook of photosynthesis. 2nd ed. New York (NY): Taylor and Francis; 2005. p. 793–809.
  • Chang L, Limin Wang C, Peng C, et al. The chloroplast proteome response to drought stress in cassava leaves. Plant Physiol Biochem. 2019; 142:351–362.
  • Xue WW, Dang XJ, Li X. Study on the technology of cassava ethanol fermentation. Liquor Make. 2005;32:39–40.
  • Wang LM, Jin X, Li QB, et al. Comparative proteomics reveals that phosphorylation of β carbonic anhydrase 1 might be important for adaptation to drought stress in Brassica napus. Sci Rep. 2016;6:39024.
  • Li YP, Huang J, Liu ZF, et al. Effects of water stress of photosynthetic characteristics of cassava seedlings. Chin J Top Crops. 2013;34:685–689.
  • Liu ZF, Huang J, Hu TR, et al. Research on photosynthetic characteristics of cassava leaf under moderate water stress. Southwest china. J Agri Sci. 2011;24:1286–1289.
  • Wang ZP, Luo XL, Meng LP, et al. Effects of different water conditions on the physiological characteristics of cassava leaves. Guangxi Agri Sci. 2010;41:419–422.
  • Yu XL, Wang G, Ruan MB, et al. Physiological and biochemical changes of leaves in different cassava varieties under water stress. Chinese Agri Sci Bulletin. 2012;28:60–64.
  • Lokko Y, Anderson JV, Rudd S, et al. Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Rep. 2007;26:1605–1618.
  • Sakurai T, Plata G, Rodríguez-Zapata F, et al. Sequencing analysis of 20,000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response. BMC Plant Biol. 2007;7:66.
  • Utsumi Y, Tanaka M, Morosawa T, et al. Transcriptome analysis using a high-density oligomicroarray under drought stress in various genotypes of cassava: an important tropical crop. DNA Res. 2012;19:335–345.
  • Fan W, Hai MR, Guo YL, et al. The ERF transcription factor family in cassava: genome-wide characterization and expression analyses against drought stress. Sci Rep. 2016;6:37379.
  • Fu LL, Ding ZH, Han BY, et al. Physiological investigation and transcriptome analysis of Polyethylene Glycol (PEG)-induced dehydration stress in cassava. Int J Mol Sci. 2016;17:283.
  • Hu W, Yang HB, Yan Y, et al. Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep. 2016;6:22783.
  • Ding ZH, Fu LL, Yan Y, et al. Genome-wide characterization and expression profiling of HD-Zip gene family related to abiotic stress in cassava. PLoS One. 2017;12:e0173043.
  • Ruan MB, Guo X, Wang YL, et al. Genome-wide characterization and expression analysis enables identification of abiotic stress-responsive MYB transcription factors in cassava (Manihot esculenta). J Exp Bot. 2017;68:3657–3672.

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