Drought-Responsive Mechanisms in Plant Leaves Revealed by Proteomics

Abstract

Plant drought tolerance is a complex trait that requires a global view to understand its underlying mechanism. The proteomic aspects of plant drought response have been extensively investigated in model plants, crops and wood plants. In this review, we summarize recent proteomic studies on drought response in leaves to reveal the common and specialized drought-responsive mechanisms in different plants. Although drought-responsive proteins exhibit various patterns depending on plant species, genotypes and stress intensity, proteomic analyses show that dominant changes occurred in sensing and signal transduction, reactive oxygen species scavenging, osmotic regulation, gene expression, protein synthesis/turnover, cell structure modulation, as well as carbohydrate and energy metabolism. In combination with physiological and molecular results, proteomic studies in leaves have helped to discover some potential proteins and/or metabolic pathways for drought tolerance. These findings provide new clues for understanding the molecular basis of plant drought tolerance.

Keywords: drought stress; leaves; molecular mechanism; proteomics.

Figure 1

Functional categories of drought-responsive protein species and unique proteins in leaves revealed by proteomic studies. (A) Protein species include all the protein isoforms generated from gene variable splicing and post-translational modifications in the original publications; (B) Unique proteins indicate the protein family whose members have similar protein sequence homology and functional domains.

Figure 2

Schematic representation of drought responsive proteins involved in signaling, gene expression regulation, protein synthesis and degradation. The solid line indicates single-step reactions, and the dashed line indicates multi-step reactions. (A) Signaling; (B) DNA replication and transcription; (C) RNA processing; (D) Protein synthesis; (E) Protein processing; (F) Protein degradation. 14-3-3: 14-3-3 protein; Nep: aspartic proteinase; ClpP: ATP-dependent Clp protease; ABP: auxin-binding protein; BiP: endoplasmic reticulum-luminal binding protein; CaB: calcium ion binding protein; CaSR: calcium sensing receptor; CDPK: calcium-dependent protein kinase; CAM: calmodulin; CNX: calnexin; CRT: calreticulin; CP: cysteine proteinase; EF: elongation factor; ERF: ethylene-responsive transcription factor; GDI: GDP dissociation inhibitor; GR-RBP: glycine-rich RNA binding protein; HSP: heat shock protein; HMG: high mobility group protein; HOP: Hsp70-Hsp90 organizing protein; AP: leucine aminopeptidase; MatK: maturase K; MEP: metalloendopeptidase; MC: molecular chaperone; OP: oligopeptidase A-like; PPIase: peptidyl-prolyl cis-trans isomerase; PLD: phospholipase D; PhyC: phytochrome C; PCNA: proliferating cell nuclear antigen; PIP: proline iminopeptidase, putative; PDI: protein disulphide isomerase; PP2C: protein phosphatase 2C; RanBP: Ran-binding protein; RT: retrotransposon protein; RNase: ribonuclease; RNP: ribonucleoprotein; RP: ribosomal protein; RBP: RNA binding protein; Hlc: RNA helicase; RNAP: RNA polymerase; SCPL: serine carboxypeptidase-like protein; STK: serine/threonine kinase; PSP: serine/threonine-protein phosphatase; SnRK: sucrose non-fermenting 1-related protein kinase; TCP: T-complex protein; TRIP1: TGF-β receptor-interacting protein 1; TF: transcription factor; TR: transcription regulator; TIG: trigger factor-like protein; V-PPase: vacuolar H⁺-pyrophosphatase; V-ATPase: vacuolar H⁺-ATPase; Zmp: zinc metalloprotease.

Figure 3

Schematic representation of drought responsive proteins involved in reactive oxygen species (ROS) scavenging, cell structure and cycle. The solid line indicates single-step reactions, and the dashed line indicates multi-step reactions. (A) ROS scavenging; (B) Cytoskeleton; (C) Cell cycle; (D) Cell wall modulation. ADF: actin depolymerizing factor; ALDH: aldehyde dehydrogenase; AsA: ascorbate; APX: ascorbate peroxidase; Exol: glucan exohydrolase; COMT: caffeic acid 3-O-methyltransferase; CCOMT: caffeoyl-CoA O-methyl-transferase; CAT: catalase; CDC: cell division cycle protein; DHAR: dehydroascorbate reductase; DHA: dehydroascorbate; GME: GDP-d-mannose-3′,5′-epimerase; GCL: glutamate-cysteine ligase; Grx: glutaredoxin; GPX: glutathione peroxidase; GR: glutathione reductase; GST: glutathione S-transferase; GSSG: glutathione disulfide; GSH: glutathione; GRP: glycine-rich protein; GLO: glyoxalase; LG: (R)-S-lactoylglutathione; MSR: methionine sulfoxide reductase; MG: methylglyoxal; MDHAR: monodehydroascorbate reductase; MDHA: monodehydroascorbate; ftsZ1: plastid division protein ftsZ1 precursor; PAE: pectin acetylesterase; PAL: phenylalanine ammonia-lyase; PG: pectin depolymerase; PGIP: polygalacturonase inhibitor; PHGPX: phospholipid hydroperoxide glutathione peroxidase; POD: peroxidase; Prx: peroxiredoxin; RGP: reversibly glycosylated polypeptide; SOD: superoxide dismutase; Trx: thioredoxin; TCTP: translationally-controlled tumor protein homolog; XI: xylanase inhibitor; XTH: xyloglucan endotransglycosylase.

Figure 4

Schematic model of drought responsive proteins involved in photosynthesis, carbon metabolism, fatty acid metabolism, and nitrogen and amino acid metabolism. The solid line indicates single-step reactions, and the dashed line indicates multi-step reactions. (A) Thylakoid reaction; (B) Calvin cycle; (C) Photorespiration; (D) Starch and sucrose metabolism; (E) Glycolysis; (F) Tricarboxylic acid (TCA) cycle; (G) Pentose phosphate pathway; (H) Nitrogen and amino acid metabolism; (I) Fatty acid metabolism. 1,3BPG: 1,3-bisphosphoglycerate; OMC: 2-oxoglutarate/malate carrier protein; MetE: 5-methyltetrahydropteroyltriglutamate-homocysteine methyltransferase; 6PG: 6-phosphogluconate; G6PDH: 6-phosphogluconate dehydrogenase; 6PGL: 6-phosphoglucono-δ-lactone; AHAS: acetohydroxyacid synthase; AH: aconitate hydratase; ACAD: acyl-CoA dehydrogenase; SAHase: adenosylhomocysteinase; ALAT: alanine aminotransferase; AGXT: alanine-glyoxylate aminotransferase; ADH: alcohol dehydrogenase; AldP: aldolase; AMT: aminomethyl transferase; AMY: amylase; AST: aspartate aminotransferase; ATPase: ATP synthase; AAC: ATP/ADP translocase; CA: carbonic anhydrase; FNR: chloroplast ferredoxin-NADP⁺ oxidoreductase; MSP: chloroplast manganese stabilizing protein; CS: cysteine synthase; Cyt b6f: cytochrome b6f complex; CCO: cytochrome c oxidase; Dic: dicarboxylate; DTC: dicarboxylate/tricarboxylate carrier; DLAT: dihydrolipoamide acetyltransferase; DHAP: dihydroxyacetone phosphate; ETCDB: electron carrier/iron ion binding protein; ENO: enolase; E4P: erythrose-4-phosphate; Fd: ferredoxin; F6P: fructose 6-phosphate; FBP: fructose-1,6-bisphosphate; FBPA: fructose-bisphosphate aldolase; G6P: glucose 6-phosphate; G1P: glucose-1-phosphate; GOGAT: glutamate synthase; GGAT: glutamate-glyoxylate aminotransferase; GS: glutamine synthetase; GAP: glyceraldehyde 3-phosphate; GAPDH: glyceraldehyde-3-phosphate dehydrogenase; GA: glyceric acid; GCS: glycine cleavage system; GDC: glycine decarboxylase; GO: glycolate oxidase; HCY: homocysteine; HPR: hydroxypyruvate reductase; IDH: isocitrate dehydrogenase; ICL: isocitrate lyase; LHCB: light-harvesting chlorophyll a/b-binding protein; LDH: lipoamide dehydrogenase; LDC: lysine decarboxylase; MDH: malate dehydrogenase; MS: methionine synthase; NDUFV: NADH dehydrogenase (ubiquinone) flavoprotein; NIR: nitrite reductase; OEC: oxygen-evolving complex protein; PEPCK: phosphoenol pyruvate carboxykinase; PEP: phosphoenolpyruvate; PGluM: phosphoglucomutase; PGA: phosphoglycerate; PGK: phosphoglycerate kinase; PGM: phosphoglycerate mutase; PRK: phosphoribulokinase; PSI: photosystem I reaction center protein; PSII: photosystem II reaction center protein; PC: plastocyanin; PDH: pyruvate dehydrogenase; DLDH: pyruvate dehydrogenase complex; PK: pyruvate kinase; R5P: ribose-5-phosphate; RPI: ribose-5-phosphate isomerase; Ru5P: ribulose 5-phosphate; Rubisco: ribulose-1,5-bisphosphate carboxylase/oxygenase; RCA: ribulose-1,5-bisphosphate carboxylase/oxygenase activase; RuBP: ribulose-1,5-disphosphate; RPE: ribulose-phosphate 3-epimerase; SAH: S-adenosyl-l-homocysteine; SAM: S-adenosylmethionine; SAMS: S-adenosylmethionine synthase; S7P: sedoheptulose 7-phosphate; SBPase: sedoheptulose-1,7-bisphosphatase; SBP: sedoheptulose-1,7-bisphosphate; SGAT: serine glyoxylate aminotransferase; SHMT: serine transhydroxymethyltransferase; SBE: starch branching enzyme; SS: starch synthase; SDH: succinate dehydrogenase; SCL: succinyl-CoA ligase; SUS: sucrose synthase; TLP: thylakoid lumen protein; TALDO: transaldolase; TKT: transketolase; Tric: tricarboxylate; TPI: triosephosphate isomerase; UDPG: uridine diphosphate glucose; UGPase: UTP-glucose pyrophosphorylase; VDAC: voltage dependent anion channel; X5P: xylulose 5-phosphate; α-KG: α-ketoglutarate.

Figure 5

A summary of signaling and metabolic pathways in leaves in response to drought stress. Drought stress activates several signaling cascades, regulates gene expression, and promotes protein biosynthesis and turnover in drought-stressed leaves. Besides, drought stress inhibits photosynthesis, photorespiration, nitrogen and amino acid metabolism, as well as the cytoskeleton and cell division. Importantly, plants enhance ROS scavenging, osmotic regulation and cell wall remodulation. In addition, plants also modulate membrane trafficking, fatty acid metabolism, carbohydrate and energy metabolism, as well as secondary metabolism to cope with drought stress.