Understanding the Responses of Rice to Environmental Stress Using

Reviews pubs.acs.org/jpr

Understanding the Responses of Rice to Environmental Stress Using Proteomics Raksha Singh and Nam-Soo Jwa* Department of Molecular Biology, College of Life Sciences, Sejong University, Gunja-dong, Gwangjin-gu, Seoul 143-747, Republic of Korea S Supporting Information *

ABSTRACT: Diverse abiotic and biotic stresses have marked effects on plant growth and productivity. To combat such stresses, plants have evolved complex but not well understood responses. Common effects upon perception of environmental stress are differential expression of the plant proteome and the synthesis of novel regulatory proteins for protection from and acclimation to stress conditions. Plants respond differently in terms of activation of stress-responsive signaling pathways depending upon the type and nature of the stresses to which they are exposed. Progress in proteomics and systems biology approaches has made it possible to identify the novel proteins and their interactions that function in abiotic stress responses. This will enable elucidation of the functions of individual proteins and their roles in signaling networks. Proteomic analysis of the responses to various stress conditions is performed most commonly using 2D gel electrophoresis and high-throughput identification by LC-MS/MS. Because of recent developments in proteomics techniques, numerous proteomics studies of rice under abiotic stress conditions have been performed. In this review, proteomics studies addressing rice responses to the major environmental stressesincluding cold, heat, drought, salt, heavy metals, minerals, UV radiation, and ozone are discussed. Unique or common protein responses to these stress conditions are summarized and interpreted according to their possible physiological responses in each stress. Additionally, proteomics studies on various plant systems under various abiotic stress conditions are compared to provide deeper understanding of specific and common proteome responses in rice and other plant systems, which will further contribute to the identification of abiotic stress tolerance factor at protein level. Functional analysis of stress-responsive proteins will provide new research objectives with the aim of achieving stable crop productivity in the face of the increasing abiotic stress conditions caused by global climate change. KEYWORDS: abiotic stress, signaling network, environmental stress, 2D-PAGE, LC-MS/MS, reactive oxygen species, stress tolerance

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INTRODUCTION Plants are frequently subjected to unavoidable environmental factors that cause abiotic stress, such as cold, heat, drought, flooding, salt, light, heavy metals, pollutants, and mechanical injury.1 Plant vigor and crop yields are markedly influenced by these abiotic stresses.2 Plants use various strategies to cope with and adapt to stress conditions; these depend on changes in levels of protein relative abundance, either by increase or decrease in protein relative abundance of stress-responsive proteins, resulting in changes at the whole proteome, transcriptome, and metabolome levels.3−5 Expression patterns at the protein and transcript levels do not always correlate due to the effects of posttranslational regulatory mechanisms such as RNA stability and protein degradation.6−8 In addition, the intensity and duration of stress can have a substantial effect on the complexity of the stress response. The phenotypic plasticity of plants, which limits damage under stress conditions, is directly related to protein abundance.9,10 Because protein−protein interactions are directly affected by stress, it is important to investigate changes in proteome networks. Advanced proteomics techniques have led to optimized experimental methods that provide a clear © 2013 American Chemical Society

understanding of gene function and phenotypic changes during stress responses.11−13 Rice, a staple food for more than half of the global population, is markedly affected by abiotic stresses, including cold, heat, drought, salt, heavy metals, UV radiation, and ozone, which compromise productivity and yield quality.14 However, recent progress in rice research in different areas such as analysis of interactome, transcriptome, and metabolome with dissection of stress regulatory networks has been proposed, providing broad platform for rice research.15−23 The study of differential changes in proteome profiles in response to abiotic stress is an approach to better understanding the physiology and molecular mechanisms that underlie rice stress responses. Furthermore, differential proteomics could contribute to the identification and characterization of novel stress-tolerance proteins that could be used as biological markers for the study of a given stress response. Over the past few decades, Special Issue: Agricultural and Environmental Proteomics Received: July 5, 2013 Published: August 28, 2013 4652

dx.doi.org/10.1021/pr400689j | J. Proteome Res. 2013, 12, 4652−4669

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Figure 1. Major abiotic stress responses in rice. Common response and defense system that are induced under major abiotic stress conditions (cold, heat, drought, salt, heavy metals, minerals, UV radiation, and ozone). All of these abiotic stresses result in the production of ROS (reactive oxygen species). An increased abundance of ROS scavenging proteins help stressed plants to detoxify ROS and maintain redox homeostasis within the cell.

Golgi membrane, and plasma membrane fractions−have been used to evaluate differential responses to cold stress.24 A differential proteomic analysis of rice seedlings exposed to a low temperature (5 °C) for 48 h revealed an increased relative abundance of proteins related to energy metabolism (adenylate kinase, putative glyoxysomal malate dehydrogenase, putative fructose-bisphosphate aldolase, and UDP-glucose pyrophosphorylase) and a decreased relative abundance of defenseresponse-related proteins (β-1-3-glucanase and phenylalanine ammonia lyase).30 This suggested that energy production was induced under cold conditions, while the abundance of defenserelated proteins decreased under long-term cold stress.30 Additionally, proteomic analysis of rice seedlings subjected to cold stress (12−14 °C) of varying duration identified changes in the abundance of histones (H2A.3, H2B.9, H3.2, and H4) and proteins involved in transport (calcium-binding protein and calmodulin-like protein 7), photosynthesis (RuBisCO LSU, chloroplastic ATP synthase, and oxygen-evolving complex), vitamin B biosynthesis (Vitamin B1, B9, and B2), and generation of precursor metabolites and energy [coproporphyrinogen-III, succinyl coenzyme A synthetase, (S)-2-hydroxyacid oxidase, fructose bisphosphate aldolase, and NADPspecific isocitrate dehydrogenase].31 Phenotypic and physiological responses to cold stress included a rolled-leaf phenotype and increased electrolyte leakage.7 Further proteomic analysis identified changes in the levels of proteins involved in processes

numerous proteomics studies of rice abiotic stress have provided valuable information for future research on rice crop improvement.11,12,24−27 In this review, we summarize and discuss studies not included in previous reviews on rice proteomic analysis that relate to major environmental stresses (cold, heat, drought, salt, heavy metals, minerals, UV radiation, and ozone) (Figure 1). Detailed information on the changes in protein relative abundance in response to the previously mentioned abiotic stress factors studied in rice using proteomic approaches to date is given in Table 1. Additionally, we address the relevance and importance of rice proteomics for understanding responses to major abiotic stresses.

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COLD Cold is a major environmental factor that significantly decreases crop productivity and quality.28 Cold stress results in cellular dehydration by decreasing water and nutrient uptake and has a substantial impact on the plant proteome.28 Because the rice plant originates from tropical South East Asia, it is susceptible to cold stress. The impact of cold on the differential expression of stress-related genes at the level of protein abundance has been extensively investigated in rice.29 Leaf blades, leaf sheaths, stems, endosperm, embryos, anthers, crowns, cultures suspension cells, roots and seedlings have all been subjected to proteomic analysis.24 In addition to studies at the whole-cell level, subcellular fractions−such as cytosolic, nuclear, mitochondrial, 4653


4654

salt

drought

heat

cold

stress

leaf blade leaf suspension-cultured cells leaf blade spikelets

12 °C for 1, 2, and 4 days 15 °C for 0, 8, 24, 48, and 96 h 6 and 15 °C for 12 h

35, 40, and 45 °C for 48 h 42 °C for 12 and 24 h 36, 44 °C for 3 days 45 °C for 24 h

35 and 30 °C

Doongara and HSC55 Nipponbare Huaidao 9

Japponica Dongjin Doongara Oryza meridionalis Oryza sativa Amaroo Taichung Native 1 Taichung 67 IR64

IRAT109 IR64 and Moroberekan Nipponbare CT9993 and IR62266 Nipponbare and Zhonghu 8 IR64 NM IR64 and Cheriviruppu NM Shanyou 10 and Liangyoupeijiu NM Wuyunjing IR64, Pokkali and Porteresia coarctata IR651 IR651

Nipponbare

Zhenshan 97B IRAT109

anther, panicle shoot and leaf root

5 °C 6 °C for 6 and 24 h 5, 10, and 15 °C for 24 h 12 °C for 4 days 12−14 °C for 48, 72, and 96 h

Jinheung Nipponbare NM Doongara Nipponbare

root root leaf root and leaf panicle

100 mM for 2 weeks 50 mM for 7 days and 75 mM for 5 days

leaf anther leaf leaf leaf peduncle tissue suspension-cultured cells anther shoot shoot

leaf

150 mM for 2 days 150 mM 200 and 400 mM for 2 h

1−9 days 5 days and rewatering 4 days drought (23 days) rewatered drought for 2 days drought (3 days) rewatered 100 mM for 1, 3, 5, and 24 h 100 mM 200 mM for 1, 6, and 12 h 100 mM for 10 days

extreme and moderate drought for 15 days and recovery for 3 and 6 days

split-root culture: (i) drought in both compartment root and (ii) drought in one compartment 20 days leaf

root leaf sheath leaf blade, leaf sheath and root suspension-cultured cells leaf leaf anther leaf

plant material

10 °C for 24 and 72 h 5 °C for 48 h 5 °C for 48 h

condition

Dongjin Nipponbare Nipponbare

cultivar

2-DE/MALDI-TOF-TOF MS/MS 2-DE/MALDI/MS

2-DE-MALDI-TOF/MS 2-DE/MALDI-TOF/TOF MS 2-DE/MALDI-TOF/MS

30 85 41 18 85

37 12 39

identified proteins

87 7 36 37 31

33 39 30

ref

1487

70

100 34 200 mM (441); 400 mM (557) 24 29

24 29

76 34 20

60 93 13 39 12 31 DIGE (106); iTRAQ (521) 25 117 9

Zhenshan 97B (17); IRAT109 (20) 982

1487

54

80 85

88 79 86

59 67 63 60 62 66 75 84 76 78

64

61

65

48

37 14 38 shoot (150); leaf (100) shoot (22); leaf (6) 32 Pro-Q diamond staining (13); Pro-Q diamond staining (13); 41 silver staining (19) silver staining (19) 63 52 53 73 48 46 139 40 47 50 50 54

30 93 60 70 label free (236); iTRAQ (85)

37 12 39

differentially expressed protein spots

Zhenshan 97B (17); IRAT109 (20) SDS-PAGE/nano LC-MS/MS LTQ-XL ion moderate (358); trap MS and NSAF extreme (245); 3 days recovery (488); 6 days recovery (579) 2-DE/MALDI-TOF/TOF 71 2-DE/MALDI-TOF-MS/ESI-TOF/MS/MS 93 2-DE/MALDI-TOF-MS 18 2-DE/MALDI-MS/ESI-Q-TOF/MS/MS 42 2D-Edman sequencing 12 2-DE/MALDI-TOF-MS 31 2D-DIGE-MALDI-TOF MS and iTRAQ DIGE (221); iTRAQ (521) 2-DE/MALDI-TOF 38 2-D-DIGE/LC-MS/MS 122 2-D-MALDI-TOF-MS/ESI-MS/MS 34

SDS-PAGE-nano LC-MS/MS (LTQ-XL ion trap MS) and NSAF 2-DE/MALDI-TOF-MS

2-DE-LC/MS/MS

2-DE/MALDI-TOF/MS 2-DE/MALDI-TOF/MS SDS-nano LC-MS/MS 2-DE/nano-LC-MS/MS

2-DE Edman sequencing; MALDI-TOF-MS 2-DE/MALDI-TOF/TOF-MS 2-DE/MALDI-TOF/ESI-MS/MS 2-DE/MALDI-TOF 2D-SCX chromatography label-free nano-LC-MS/MS and iTRAQ nano-LC-MS/MS 2-DE/MALDI-TOF, Edman sequencing TMT labeling and nano-LC-MS3 2-DE/MALDI-TOF/TOF-MS

2-DE/MALDI-TOF/ESI-MS/MS 2-DE/MALDI-TOF/MS 2-DE/MALDI-TOF/ESI-MS/MS

separation and identification method

Table 1. List of Differentially Expressed Rice Proteome in Response to Various Abiotic Stress Conditionsa

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condition

50 mM for 7 days 130 mM for 4 days 150 mM for 24, 48, and 72 h 150 mM for 0, 10, and 24 h

cultivar

IR4630-22-2-5-1-3 Nipponbare Nipponbare Nipponbare

leaf blade leaf root root

plant material 2-DE-MALDI-TOF/TOF-MSMS/MS 2-DE/nanoESI-LC-MS/MS 2-DE/MALDI-TOF/MS (I) 2-DE/Pro-Q diamond dye/ABI 4700 Proteomics analyzer; (II) 2-DE/SYPRO ruby dye/MALDI-TOF/TOF 2-DE-Edman sequencing

separation and identification method

4655

a

identified proteins

25 24 23 37 32

23 52 32

23 14 25 22

37 14 25 33

34 39

60

87

16 29 34 79 17 13

21 21 36 27 41 [16 (leaf) and 25 (roots)]

30 27 36 27 92

16 50 34 79 17 13

8

11 33 28 (I) 28; (II) 31

8

32 55 54 (I) 38; (II) 44

differentially expressed protein spots

To the best of our knowledge all of the published papers to date on the rice proteomic analysis in major abiotic stresses have been included. NM, not mentioned.

Nipponbare, IR36 and Pok- 50, 100, and 150 mM for 6 to 48 h leaf sheath kali Baldo 0, 10, and 100 μM for 15 days root 2-DE/MALDI-TOF/MS Hwayeong 0.2 to 1.0 μM for 4 days seed and shoot 2-DE/MALDI-TOF/MS cadmium Dongjin 100 μM for 24 h root and leaf 2-DE/MALDI-TOF/MS Dongjin 0, 0.1, 0.5, or 1.0 mM for 48 h root 2-DE/MALDI-TOF/MS nitrous Xiushui63 0.1 mM and 0.005, 0.05, 0.1, and 0.2 mM of SNP leaf and root 2-DE/MALDI-TOF/MS oxide and (sodium nitroprusside) for 8 days cadmium silicon and Jefferson Si (0.0 or 0.6 mM) Cd (0 or 10 μM) leaf 2-DE/MALDI-TOF/TOF/MS cadmium Dongjin 0, 50, and 100 μM for 4 days root 2-DE/MALDI-TOF/MS arsenic Dongjin 0, 50, and 100 μM for 4 days leaf 2-DE/MALDI-TOF/MS and ESI-MS/MS mercury TN67 25 μM for 3 h root 2-DE/ESI-MS/MS cadmium, Nipponbare 250 μM for 72 h leaf 2-DE Edman sequencing cobalt, copper, mercury, lithium, strontium, zinc Wuyunjing no. 7 200 μM for 6 days germinating embryo 2-DE/MALDI-TOF/MS copper Hwayeong 0.2, 0.5, 1.0, 1.5, and 2 mM for 4 days germinating seed with shoot 2-DE/MALDI-TOF/MS B1139 and B1195 8 μM for 3 days root 2-DE/MALDI-TOF/MS Kasalath and Koshihikari 0 and 50 μM for 24 and 72 h root 2-DE/MALDI-TOF/TOF-MS aluminum Xiangnuo 1 (XN1) 2 mM (pH 4.3) for 3 days root 2-DE/MALDI-TOF/TOF/MS/MS Oryza sativa “Guara” and 1 and 50 μM for 4 days leaf 2D IEF/SDS-PAGE, 2D BN/SDS-PAGE, manganese Hordeum vilgare “BaronLC-MS/MS ess” phosphorus Nipponbare and NIL6-4 1 and 100 μM phosphorus root 2-DE/MALDI-TOF/TOF-MS Lemont and Dular natural light and enhanced ultraviolet for leaf 2-DE/MALDI-TOF/MS 1, 7, and 14 days ultraviolet radiation 93−11 0.67 W m-2 UVB and leaf 2-DE/MALDI-TOF/MS 0.28 W m-2 UVA for 6, 12, and 24 h Nipponbare 200 ppb for 3 days leaf 2-DE-Edman sequencing ozone Nipponbare 0.2 ppm for 24 h leaf 2-DE-nESI-LC-MS/MS

stress

Table 1. continued ref

10 4

129

120 128

111 110 112 115 114 118

102 103 106 93

100

95 97 94 96 101

72

89 74 73 83

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Figure 2. General scheme of various cellular and defense mechanisms that are triggered under various abiotic stress conditions. Abiotic stresses [(A), cold (B), heat (C), drought (D), salt (E), heavy metals (F), minerals (G), UV radiation, and (H) ozone] altered various cellular responses in rice resulting in the generation of ROS with altered homeostasis. Common cellular responses to all abiotic stresses are shown in the same color boxes such as photosynthesis (green), redox homeostasis (red), and metabolism (light green). Unique responses under each stress are shown by blue color boxes. Furthermore, abiotic stress factors activate detoxification/defense mechanisms, regulatory proteins, and chaperones in plants, which might work cooperatively to establish a new homeostasis and enhanced stress tolerance. 4656



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finding that cold treatment in the young microspore stage induced the partial degradation of β-expansin and glycogen phosphorylase in the trinucleate stage may contribute to a full understanding of cold-induced male sterility in rice.37,38 However, it should be noted that changes in protein abundance depend upon multiple factors, including the duration of cold treatment, plant growth stage, water supply, severity of cold stress, and so on. Several proteomic analyses of rice seedlings revealed that cold stress also affected post-translational modifications, such as glycosylation and phosphorylation.39−41 Changes in the glycosylation and phosphorylation patterns of calreticulin protein showed that N-glycosylated proteins were also affected by cold stress, confirming an effect on posttranslational modification in rice.39 A number of phosphoproteins, including enolase, glyceraldehyde-3-phosphate dehydrogenase, nucleoside diphosphate kinase, ascorbate peroxidase, adenosine kinase, CPK1 adaptor protein 2, ATP synthase subunit α, methionine synthase 1, and tubulin, were also cold-responsive and found to be involved in redox homeostasis, signal transduction, and metabolism.41 The phosphorylation of four proteins, glyoxalase-I, calmodulin-related protein, calreticulin, and an unknown protein, was increased by cold treatment.42 It is evident from these studies that posttranslational modification is also regulated by cold stress in rice leaf sheaths and roots.39,41 Cold stress induces tissue-specific proteome patterns. The similarity of the proteome patterns exhibited by rice leaf sheaths and leaf blades in response to cold might be due to the presence of chloroplasts and proteins related to photosynthesis and energy production.30 In contrast, a completely different proteome pattern was identified in root tissue.30 Roots and leaf sheaths have some commonality in cold responses, as suggested by the decrease in relative abundance of 5-methyltetrahydropteryltriglutamate-homocysteine S-methyltransferase (enzymatic reaction catalyzed by 5-methyltetrahydropteryltriglutamate-homocysteine S-methyltransferase: 5-methyltetrahydropteroyltri-Lglutamate + L-homocysteine ⇌ tetrahydropteroyltri-L-glutamate + 30 L-methionine) in both tissues. However, the decrease in relative abundance of calreticulin in leaf sheaths and leaf blades and the increase in relative abundance of UDP-glucose pyrophosphorylase (enzymatic reaction catalyzed by UDP-glucose pyrophosphorylase: glucose-1-phosphate + UTP ⇌ UDP-glucose + pyrophosphate) in roots and leaf blades indicates the presence of a complex cold response mechanism in rice.30 Transmembrane-domain-containing proteins were identified by proteomic analysis of rice root cell plasma membranes. Cold-shock protein relative abundance was significantly decreased, suggesting that this protein plays a negative role during cold stress.43 Root plasma membrane proteomics identified previously undetected proteins with functions in cell growth and division.43 The major effects of cold stress are on photosynthetic apparatus, antioxidant system, post-translational modification, energy and metabolism, defense, protein metabolism, and sugar signaling (Figure 2A). Unique proteome responses under cold stress are vitamin B biosynthesis, histone modification, catalase activity, and vesicle trafficking (Figure 2A). Further organelle-specific changes in the proteome caused by cold stress have also been described.30,43 Further understanding of the regulatory mechanisms of the above responses will provide important information for genetic engineering of cold-tolerant rice varieties.

such as signal transduction (putative protein phosphatase 2Clike protein, protein similar to WAK1, putative armadillo repeat-containing protein, and RAB2A), RNA processing (PPR containing protein), translation and protein processing [putative nascent polypeptide-associated complex (NAC) α chain, elongation factor 1-β′, putative acidic ribosomal protein P3a, and heat shock proteins], redox homeostasis (peroxidases, thioredoxin H-type, and NADP-malate dehydrogenase), photosynthesis and photorespiration (glycine dehydrogenase P and RcbA), and metabolism of carbon (enolase, putative 2,3bisphosphoglycerate-independent phosphoglycerate mutase and putative aconitate hydratase), nitrogen (ferredoxin-nitrite reductase and glutamine synthetase shoot isozyme), sulfur (putative plastidic cysteine synthase 1 and S-adenosylmethionine synthetase 2), and energy (adenylate kinase A, ATP synthase α and β chains), hormone response [SAPK3 (serine/ threonine-protein kinase) and lipoxygenase (LOXs)], and osmotic stress association as well as the possible role of sugar sensing (sucrose synthase and vacuolar invertase) that might function cooperatively to maintain homeostasis during cold stress.7,32 Several novel cold-responsive proteins were identified; these included 2-cys peroxiredoxin, armadillo repeatcontaining protein, and putative nascent polypeptide-associated complex α chain.7 Proteins involved in energy production (pyruvate orthophosphate dikinase precursors (PPDK), aconitate hydratase, glycine dehydrogenase and enolase), metabolism (putative phosphogluconate dehydrogenase, NADPspecific isocitrate dehydrogenase, putative fructokinase, and cytoplasmic malate dehydrogenase), vesicular trafficking (α-soluble NSF attachment protein), detoxification (glyoxalase I and oxalylCoA decarboxylase), and several other cellular processes (actin and PrMC3) were increased in protein-relative abundance in rice root tissue in response to cold stress. These data will allow a better understanding of the molecular basis of cold stress responses in rice roots.33 An important finding of Yan et al.7 was the degradation of the photosynthesis-related protein, RuBisCO LSU, upon cold treatment, suggesting that a decrease in the rate of photosynthesis was correlated with the physiological responses to cold stress.7 Other studies have also indicated that cold stress affects photosynthesis.7,30,34,35 The majority of the differentially expressed proteins (44%) were chloroplast-localized (chaperonin α and β subunit, ATP synthase CFI α chain, putative thiamine biosynthetic enzyme, PSII oxygen-evolving complex protein 2, HSP 70, and putative ferredoxin-NADP(H) oxidoreductase), implying that the chloroplast is the main organelle affected by cold stress.36 The major and minor groups of proteins responsive to cold were found to be involved in protein metabolism (eukaryotic initiation factor 4A, translational elongation factor Tu, FtsH-like protein, and HSP 70) and cell-wall component biosynthesis proteins (sucrose synthase 1 and 2, methionine synthase, and glutamate semialdehyde aminotransferase), respectively.36 Short-term exposure to cold stress caused an increase in relative abundance of UDP-glucose pyrophosphorylase (UGPase) and sucrose synthase 1, which are involved in the TCA cycle, suggesting that cold stress alters the abundance of proteins involved in carbohydrate metabolism.36 Additionally, proteins related to antioxidative/detoxifying reactions (ferritin, GDP-mannose 3′, 5′-epimerase, 6-phosphogluconate dehydrogenase, and GST) and energy pathways (α and E chains of ATP synthase CF1 and ATPase α subunit) were identified, suggesting that a complex protein network within rice leaf cells mediates the response to cold stress.36 The 4657



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high temperatures and chaperonin 60 β precursor, were increased in relative abundance.53 These results suggested a role for these proteins in maintaining the photosynthetic machinery in rice seedlings during heat stress.53 Increased relative ion leakage and lipid peroxidation during heat stress suggested that high temperature causes oxidative stress in rice leaves.46 Dehydroascorbate reductase, which is involved in the antioxidation pathway in plants, was increased in relative abundance at high temperatures (35, 40, and 45 °C), with the highest levels of induction at 40 and 45 °C, implying that rice defense mechanisms were activated in accordance with the increase in temperature.53 Indeed, HSP 70 and sHSPs were activated at 45 °C, suggesting that rice can tolerate such temperatures.53 Rice plants respond differently depending upon heat stress intensity.53 Lignification-related proteins, such as class III peroxidase and phenylalanine ammonia-lyase (PAL), were decreased in relative abundance by treatment at 35 and 40 °C, indicating that lignification is decreased by exposure to high temperatures.53 Heat stress caused the induction of proteins related to photosynthesis (RuBisCO activase large isoform), photorespiration (glycine dehydrogenase P), Calvin cycle (chloroplastic phosphoglycerate kinase, transketolase, PRK, and chloroplastic sedoheptulose-1,7-bisphosphatase), thiamine biosynthesis (thiamine biosynthesis protein 1), and defense (HSP70, Cpn60, and HSP90), suggesting that these proteins are directly linked to physiological aspects of thermo-tolerance in Oryza meridionalis.54 A decrease in relative abundance of photosynthesis-related enzyme ferredoxin NADP(H) oxidoreductase suggests that heat stress inhibits electron transport in Oryza meridionalis.54 About 35% of proteins that were increased in relative abundance by heat stress, including transketolase, UDP-glucose pyrophosphorylase, putative thiamine biosynthesis protein, and pyruvate dehydrogenase, were related to energy and metabolic pathways, implying that these pathways are significantly impacted by heat stress and that plants require large amounts of energy to cope with heat stress.46 Proteomic analysis of the effect of heat stress on rice caryopsis development showed that waxy proteins, allergen-like proteins, and elongation factor 1β were decreased in relative abundance, but sHSP, glyceraldehyde-3-phosphate dehydrogenase, glutelins, and prolamin were increased in relative abundance, providing important information for understanding of rice caryopsis proteins and the improvement of the quality of grain exposed to heat stress.48 An increase in relative abundance of high-molecular-weight waxy protein (granule-bound starch synthesis) in TN1 and IR36 varieties was correlated with the high amylose content.48 In contrast, granule-bound starch synthase decreased in relative abundance in TNG 67 variety upon heat stress, resulting in less amylose content.48 Phosphorylation and glycosylation of waxy proteins and glutelins were observed using LC-MS/MS analysis in caryopsis development.48 However, detailed analysis is needed to confirm the phosphorylation and glycosylation of rice waxy proteins to identify the possible role of post-translational modification on caryopsis development in rice. In conclusion, an increase in the relative abundance of HSPs, sHSPs, proteins related to energy and metabolism, and antioxidant enzymes and a decrease in relative abundance of photosynthesis-related proteins, lignification-related proteins, and waxy proteins occur in response to heat stress (Figure 2B).

HEAT Heat stress is associated with a substantial decrease in transcription and translation due to protein misfolding and denaturation of several intracellular proteins and membrane complexes.44 Heat stress leads to the induced expression of several heat-shock proteins (HSPs). However, proteomic analysis of rice subjected to heat stress revealed several other proteins that are critical for adaptation to high temperature; these have been reviewed elsewhere.45,29 Proteomic analysis of rice seedlings subjected to 42 °C for 12 and 24 h identified changes in the levels of HSPs (HSP 70, HSP 100, sHSPs, and chaperonin 60 β-precursor), regulatory proteins [chloroplast elongation factor Tu, cysteine proteinase, subunit α Type 1, and putative α 1 subunit of 20S proteasome, nucleoside diphosphate kinase 1 (NDPK1)], and other proteins involved in energy metabolism [transketolase, UDP-glucose pyrophosphorylase, putative thiamine biosynthesis protein, phosphoribulokinase (PRK), and pyruvate dehydrogenase], and redox homeostasis [glutathione S-transferases (GST), dehydroascorbate reductase (DHAR), thioredoxin h-type (Trx h), chloroplast precursors of superoxide dismutase (SOD), FAD-binding domain containing protein like, putative Bplo, and glutathione reductase (GR)].45,46 Similar changes in heat-responsive proteome patterns, including changes in the abundance of HSP70, the DnaK-type molecular chaperone BiP, HSP100, and chaperonin 60 β precursor, have been reported in cultured rice cells.47 Heat-responsive proteins were involved in protein metabolism (putative eukaryotic translation initiation factor 3 subunit 8, elongation factor 1-γ 3 and putative glycyl-tRNA synthetase, exopeptidases such as putative glutamate carboxypeptidase, putative carboxypeptidase D, putative prolyl carboxypeptidase-like protein, putative serine carboxylase II-2, putative puromycin-sensitive aminopeptidase or metalloproteinase MP100, and endopeptidases such as putative cysteine proteinase, putative xylem serine proteinase 1 precursor and proteolytic subunit of ATP-dependent Clp protease), carbohydrate metabolism (succinate dehydrogenase, phosphoglucose isomerase, phosphofructokinase, glyceraldehyde 3-phosphate dehydrogenase, enolase, and phosphoglycerate mutase), transport (probable aquaporin tonoplast intrinsic protein 3−1, eukaryotic porin family protein, and voltagedependent anion-selective channel protein), and stress response (Clathrin, FAD-binding domain containing protein like, putative Bplo and glutathione reductase).47 In addition to HSPs, small heat-shock proteins (sHSPs) were also highly induced in rice leaves by heat stress; these proteins play a crucial role in heat tolerance by restoring normal protein conformation and cellular homeostasis.46 Induction of sHSPs in heat-tolerant varieties was identified by several proteomics studies, suggesting that these proteins could serve as a marker of heat tolerance.48−50 The heatresponsive protein expression pattern differs among rice genotypes; some thermo-tolerant species showed accumulation of high levels of heat-responsive proteins, such as sHSPs.51 Both heat-sensitive and heat-tolerant rice seedlings exposed to temperatures higher than 40 °C for long periods show significantly decreased activity and quantities of RuBisCO.52 Decreased relative abundance of photosynthesis-related enzymes such as PRK and RuBisCO by heat stress suggested that the rate of photosynthesis was reduced by heat treatment.46 Disruption of photosynthesis by heat stress was further supported by a proteomics study of rice seedlings exposed to temperatures of 35, 40, or 45 °C, which reported that RuBisCO activase precursor, an enzyme that inhibits photosynthesis at

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DROUGHT Drought is associated with low water availability and cellular dehydration and is one of the major factors limiting crop 4658



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productivity.55 Drought-tolerant plants can maintain water balance within the cell, survive with a low water content, and recover quickly after rewatering.56 Proteome changes in response to drought have been investigated extensively in plants.29,57 Plant survival and growth during drought stress may be due to increase in relative abundance of proteins related to protein folding and assembly (HSP 70, putative DnaK-type molecular chaperone BiP, and putative chaperonin 60 β) and elimination of unnecessary protein biosynthesis due to decrease in relative abundance of proteins related to translation (elongation factors, ribosomal proteins, and nucleic acid binding protein).58,59 Proteomic analysis of 3-week-old seedlings of drought-tolerant rice cultivars CT9993 (upland) and IR62266 (lowland) identified 42 differentially abundant spots, the relative abundance of 27 of which differed between the cultivars.60 Additionally, 15 proteins showed similar relative abundance patterns in both cultivars, that is, increase in relative abundance of 11 and decrease in relative abundance of 4 proteins during drought stress. Sixteen droughtresponsive proteins were identified in the CT9993 and IR62266 cultivars.60 Comparison of the proteomes of the droughtsusceptible cultivar Zhenshan97B and the tolerant cultivar IRAT109 during drought stress showed different proteome profiles. The differences included marked increases in relative abundance of oxidation−reduction proteins [chloroplast Cu−Zn superoxide dismutase (SOD) and dehydroascorbate reductase] in IRAT109, suggesting the induction of an antioxidant system to protect plants from damage during drought stress.61 Proteins such as actin depolymerizing factors, translational initiation factor EF-Tu, and RuBisCO activase isoforms were increased in relative abundance by drought stress, but isoflavone reductase-like protein was decreased in relative abundance. This suggests that actin depolymerizing factors, translational initiation factor EF-Tu, and RuBisCO activase isoforms play crucial roles in drought tolerance.60,62 LEA-like protein and chloroplast Cu−Zn SOD were increased in relative abundance, but Rieske-FeS precursor protein was decreased in relative abundance in rice leaf cells by drought stress.63 The levels of most drought-responsive proteins recovered to those in well-watered control plants within 10 days of rewatering.60 Proteomic and physiological studies of rice during moderate drought and extreme drought and during the recovery stage identified different protein patterns for each condition, with degradation of most of the drought-responsive proteins during extreme drought.64 Proteins involved in signaling and transport (small G-proteins, putative GTP-binding protein Rab7, putative GTP-binding protein Rab7a, small GTPase Rab2a and Ras-related protein Rab11C, aquaporins, V-ATPase proteins, and vacuolar proton pump subunit D) were increased in relative abundance during severe drought; most were degraded during recovery, suggesting that water transport and drought signaling are important elements in the drought response in rice and thus might be key to the understanding of drought tolerance.64 Root characteristics have significant effects on plant responses to drought. Quantitative label-free shotgun proteomic analysis of partially dried and well-watered rice roots in split-root systems identified altered expression of 38% of proteins (peroxidase, SODs, catalase, ascorbate peroxidase, glutathione reductase, putative pathogen-induced protein 2−4, Win1-pathogenesis-related protein, HSP 101, putative GTPbinding protein, Ras related protein Rab 11D, and small GTP binding protein Rab5) in the partially dried roots relative to the control.65 Differences in protein expression patterns between

partially dried and well-watered roots might be due to the effects of drought-induced, long-distance hormonal signals mediated by ABA or cytokinin or by direct hydraulic effects of adjacent roots. An increase in relative abundance of stressresponsive proteins (PRs and sHSPs), oxidation−reduction proteins (superoxide, catalase, and peroxidase), and lipid metabolism proteins (isoprenoid biosynthetic pathway and isoprenoid compounds) and a decrease in relative abundance of transport proteins (small G proteins and mitochondrial import proteins) and signaling proteins (14-3-3 protein and GF14-E) was observed during drought stress.65 The rice reproductive mechanism is also affected by drought stress.66 Comparison of the proteomes of rice anther cells of the IR64 and Moroberekan genotypes in response to drought might provide information on the reason for the difference in spikelet fertility between the two genotypes.67 Moroberekan had a greater recovery capability after rewatering (β-expansin and putative actin binding protein), and anther development (cysteine protease) was less affected compared with the drought-sensitive genotype IR64 during drought stress.67 The difference in the recovery capacity of the two genotypes suggests an explanation for their different sensitivities to drought.67 Assessment of the effects of drought treatment on rice seedlings by proteomic (2D gel electrophoresis coupled with MALDI-TOF/TOF), mRNA (cDNA microarray) and metabolite (GC-MS) analyses resulted in identification of markedly different protein, transcript, and metabolite patterns.59 For example, expression of nucleic acid and lipid metabolismrelated genes was not detected at the protein level, and the expression of most genes involved in metabolic and biosynthetic pathways differed markedly at the mRNA level compared with the proteins level.59 Post-translational modification is also altered by drought stress, as indicated by the identification of 10 phosphoproteins (NAD-malate dehydrogenase, abscisic acid- and stress-inducible protein, ribosomal protein, drought-induced S-like ribonuclease, ethylene-inducible protein, guanine nucleotide-binding protein β subunit-like protein, and germin-like protein 1) affected by drought stress.63 Similarly, Ali and Komatsu reported the identification of 10 proteins (SOD, light harvesting complex chain II, photosystem II oxygen-evolving complex protein, oxygen-evolving enhancer protein 2 (OEE2), chloroplast ATPase, serine hydroxylmethyltransferase I, 2-Cys peroxiredoxin, actin depolymerizing factor, and phosphoglucomutase cytoplasmic 2) with an increased abundance and 2 proteins (RuBisCO LSU and SSU) with a decreased abundance in leaf sheaths of 2-week-old rice seedlings exposed to drought stress for 2−6 days.62 These drought-responsive proteins were categorized into defense, energy, metabolism, and signal transduction functional groups, suggesting the existence of a complex drought regulatory mechanism in rice.62 Drought stress affects primarily signaling and transport proteins, oxidation−reduction proteins, lipid metabolism proteins, and phosphoproteins. Additionally, using the split-root system, drought stress was shown to induce remote signaling to adjacent roots.65 A general scheme of differentially regulated proteins in rice under drought stress is shown in Figure 2C.

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SALT Salt stress is another important limiting factor for agricultural yield on newly reclaimed land and in hot, semiarid regions.68 Water uptake by roots decreases significantly with increased concentrations of NaCl and other salts, such as K+, Ca2+, 4659



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(NO3)−, and (SO4)2− in the soil.68,69 The primary effect of an increased NaCl concentration in soil water is osmotic stress and an imbalance in intracellular ion homeostasis.55,69 A secondary effect is excess ion accumulation in shoots and leaf blades, resulting in photoinhibition and cell death.55,70 Advances in functional genomics techniques such as genomics, transcriptomics, metabolomics, and proteomics have enabled the researchers to investigate salt tolerance mechanisms in cereals.71 Abbasi and Komatsu showed that salt-responsive proteins [fructose bisphosphate aldolases, photosystem II (PSII) oxygen-evolving complex protein, OEE2, and SOD] in leaf sheaths, leaf blades, and roots were increased in relative abundance when exposed to low levels of salinity stress for a short period but were drastically decreased in relative abundance after extended exposure, possibly due to the imbalance in intracellular ion homeostasis caused by continuous excessive ion uptake.72 Differential expression of triosephosphate isomerase, enolase, UGPase, and COX6b-1 suggested the activation of the energy production pathways required by plants during salt stress due to disruption of enzyme activities and basic metabolism.73 The majority of differentially abundant proteins during salt stress function in major photosynthetic metabolic processes (RuBisCO, fructose 1,6-bisphosphate aldolase, glycine dehydrogenase, and glycine hydroxymethyltransferase) and in oxidative damage processes (ascorbate peroxidase and lipid peroxidase).74 Similar results were obtained from proteomic and metabolomic analyses of rice cells in suspension culture exposed to salt stress. This supports the notion of a relationship between the enzymes involved in carbohydrate and energy metabolism and the increased production of antioxidants that mediate maintenance of cellular homeostasis.75 Reactive oxygen species (ROS) scavenging is an important aspect of salt stress. An increase in relative abundance of ROSscavenging enzymes such as peroxidases and a down-regulation of peroxidases 12, peroxidase 52 precursor, and peroxidase 43 may maintain the equilibrium between excess ROS detoxification and ROS production within the cell.73,76,77 SOD was shown to be increased in relative abundance not only by salt but also by cold, ABA, and drought, suggesting a role in the response to a variety of stress conditions.72 Transgenic seedlings overexpressing the cyclophilin OsCYP2 showed improved tolerance to salt stress, with an increased antioxidant enzyme activity and a decreased lipid peroxidation.78 These findings indicate a role for OsCYP2 in preventing oxidative damage to photosynthesis. OsCYP2 might be involved in electron transfer processes. However, further studies are required to confirm this finding.78 Rice plant tissues exhibit distinct changes in protein relative abundance. An increase in relative abundance of OEE2, aldolases, and PSII oxygen-evolving complex was detected in only leaf sheaths and leaf blades; in contrast, an unidentified protein and SOD were detected in leaf sheaths and roots.72 Proteomic analysis of apoplasm identified salt-responsive proteins involved in carbohydrate metabolism, oxido-reduction, and protein processing and degradation under salt stress at different time points.76 In contrast, analysis of the proteome associated with the plasma membranes of rice root cells under salt stress identified a novel leucine-rich-repeat-type receptorlike protein kinase, OsRPK1, and other proteins involved in important physiological processes such as membrane stabilization, ion homeostasis, and signal transduction.79 However, there was no correlation between the levels of proteins in the

rice plasma-membrane-associated proteome and gene expression at the mRNA level in response to salt stress.80 Proteomic analysis of rice roots during salt stress revealed 10 saltresponsive proteins, including six novel proteins (UGPase, COX6b-1, GS root isozyme, putative α-NAC, putative splicing factor-like protein, and putative ABP) and four proteins reported previously [triosephosphate isomerase, enolase, SAMS2 (S-adenosylmethionine synthetase 2), and peroxidase]. Thus further functional analysis of the roles of these proteins in salt tolerance is warranted.73 The mRNA abundance and activity of enolase were significantly increased in rice by various stresses, but the enolase protein level was decreased in relative abundance, suggesting that enolase is regulated at the transcriptional, post-transcriptional, translational, and posttranslational levels.73,81,82 Salt treatment led to increased phosphorylation of cytoplasmic malate dehydrogenase and calreticulin, suggesting carbohydrate metabolism and Ca2+ signaling processes as a major phosphorylation cascade in rice under salt stress.42 Chitteti and Peng studied the differential changes in rice roots phosphoproteome using Pro-Q Diamond staining during an early phase (10, 24 h) under salt stress.83 Phosphorylation patterns of numerous proteins have been differentially regulated under salt stress including GST, small GTP binding protein, transposase, DnaK-type Hsp70, putative disease-resistance protein, and putative retroelement.83 Proteins involved in anther wall remodeling (dirigent-like protein and α-L-arabinofuranosidase/β-D-xylosidase isoenzyme ARA-I) and metabolism (fructokinase-2 protein and glyceraldehyde 3-phosphate dehydrogenase) were also identified by proteomic analysis of rice anthers in salt stress.84 However, proteomic analysis of young panicle identified high accumulation of proteins related to antioxidants (ascorbate peroxidase and DHAR), regulatory (Sti1, GR-RBP, and putative r40c1 protein), signal transduction (guanine nucleotide-binding protein), and ATP generation (triosephosphate isomerase, dihydrolipoamide dehydrogenase, and cytosolic malate dehydrogenase).85 Another interesting observation is the involvement of the auxin/IAA pathway in salt stress.75 The decreased abundance of ubiquitin-conjugating enzyme E2 and IAA-amino acid hydrolase in response to salt stress further supports the involvement of the auxin/IAA pathway in the salt stress response.75 The effect of salinity has also been investigated in halophytic (salt-tolerant) rice using various proteomics approaches. Physiological studies conducted on wild halophytic rice Porteresia coarctata in comparison with Oryza sativa (IR64 and Pokkali) exposed to various salt concentrations (200 and 400 mM) showed a higher biomass and K+/Na+ ratio and an increased photosynthetic performance in halophytic rice.86 Furthermore, these physiological responses were correlated with proteomics data that indicated induction of a high proportion of newly synthesized salt-responsive proteins (alcohol dehydrogenase 1, CP47, cellulase synthase, sucrose synthase, HSP70, and glutamine synthetase) in Porteresia coarctata with increasing salt concentration. In contrast, no new proteins were synthesized in Oryza sativa (IR64 and Pokkali) under salt stress. These proteins might play key roles in the salt tolerance of Porteresia coarctata and could be targets for genetic engineering of salt-tolerant crops. Newly identified saltresponsive proteins were categorized into diverse functional groups, including photosystem function, RuBisCO activation, osmolyte synthesis, cell-wall synthesis, and chaperones.86,88,89 Salt-stress affects photosynthetic metabolism, antioxidant systems, the auxin/IAA pathway, and post-translational 4660



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glutathione reductase, putative glutathione S-transferase OsGSTU4, putative glutathione S-transferase OsGSTU12, putative glutathione S-transferase OsGSTU3, and L-ascorbate peroxidase 1) in roots under Cd stress were related to oxidative damage, but only two oxidative stress-related proteins (peroxidase and putative ferredoxin-NADP(H) oxidoreductase) were highly accumulated in leaves.94 In addition to proteins related to carbohydrate metabolism (enolase, α-1,4-glucan-protein synthase, and putative UDP-glucosyltransferase), amino acid metabolism (formyltetrahydrofolate synthetase and branched-chain amino acid aminotransferase-like), protein metabolism (putative ubiquitin isopeptidase T, chloroplast translational elongation factor Tu, and elongation factor P), pathogenesis (endo-1,3-β-glucanase), and photosynthesis-related proteins (probable photosystem II oxygenevolving complex protein 2, RuBisCO activase) were also differentially regulated in root and leaf tissues after Cd treatment.94 The proteomic response of 4-day-old rice seedlings to 0.8 mM Cd indicated marked accumulation of regulatory proteins, including receptor-like protein kinase (RLK), DnaK-type molecular chaperone BiP, pentatricopeptide (PPR) repeatcontaining-like proteins, putative retro-element, and Ulp1 protease-like proteins and stress- and detoxification-related proteins, such as putative disulfide isomerase, myosin heavy chain-like protein, putative aldose reductase glyoxalase I, and peroxiredoxin.97 These results from germinating rice seeds exposed to Cd stress suggest the possibility of establishment of new homeostasis by regulatory and stress- and detoxificationrelated proteins during Cd stress. Previously, it was reported that silicon (Si-induced Cd tolerance in rice.98,99 Proteomic analysis of the effects of Si on rice leaf proteomes under Cd stress identified differentially regulated proteins, including reduced homeostasis, regulation/ protein synthesis, pathogen response, and chaperone activity proteins.100 Interestingly, Class III peroxidase and a thaumatinlike protein were highly accumulated under Si treatment only, whereas disulfide isomerase, HSP70 homologue, NADHubiquinone oxidoreductase, and a putative phosphogluconate dehydrogenase were highly accumulated in the presence of both Si and Cd, providing important information regarding the molecular mechanisms involved in Si-induced Cd tolerance in rice.100 Similarly, under Cd stress, nitric oxide (NO) plays an important role in the alleviation of rice growth inhibition as well as differential regulation of carbohydrate metabolism (glyceraldehyde-3-phosphate dehydrogenase B and phosphoglycerate kinase, fructokinase II), secondary metabolism (PAL, putative isoflavone reductase, and orthophosphate dikinase), signal transduction (putative cysteine conjugate β-lyase), and oxidative stress-related proteins (putative ferredoxin-nitrite reductase).101 In summary, Cd stress affects proteins of photosynthetic apparatus, transporter proteins, metabolic enzymes, regulatory proteins, oxidative stress-related proteins, pathogenesis-related proteins, and carbohydrate-, amino-acid-, and protein-metabolism-related proteins (Figure 2E).

modification (Figure 2D). Further proteomic analysis of rice under salt stress will provide useful information regarding the changes in patterns of protein relative abundance; this will facilitate both an increased understanding of salt tolerance and genetic engineering of salt-tolerance traits.

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RESPONSES OF RICE PROTEOME TO HEAVY METAL STRESS Heavy metals, major environmental stressors, are naturally occurring elements with metallic properties and a specific gravity greater than 5. At the optimum concentration, heavy metals play crucial roles in plant metabolism, growth, and development.90 However, high concentrations of these metal ions lead to toxicity and cellular damage in plants.90 The responses of rice proteins toward metal stress and toxicity are influenced by the type and concentration of metals as well as the developmental stage and tissue type. Proteomics studies addressing the effects of heavy metals have been conducted in rice and other plants.29,91,92 Cadmium

The first study of the rice proteome under heavy metal stress, including cadmium (Cd), was conducted by Hajduch et al.93 Photosynthetic apparatus is severely damaged by Cd stress, as shown by degradation or fragmentation of the RuBisCO LSU after Cd stress for 72 h.93 Furthermore, the relative abundance of the OEE2 protein was decreased drastically by Cd. However, the relative abundance of photosynthesis 11 and 23 kDa proteins, RuBisCO activase precursor fragment, OsPR5, and OsPR10 proteins increased after Cd treatment.94 These results strongly suggest that Cd downregulates the photosynthetic process in rice. Several transporter proteins, such as the ABC transporter, Nramp protein, and metabolic enzymes, such as ALT and hexokinase, were relatively highly accumulated when plants were exposed to 10 μM Cd but to a lesser extent when treated with 100 μM Cd, suggesting the possibility of activation of a defense mechanism at low concentrations of Cd, whereas there was an inhibition of plant development at high concentrations in rice roots.95 The relative abundances of regulatory proteins, including cytokinin oxidase and ER1-like receptor kinase and metabolic enzymes, such as cinnamyl alcohol dehydrogenase, were increased, but those of cyclin family proteins were decreased.95 The relative abundances of methionine synthase and phosphoglucomutase (PGM) decreased with 0.1 mM CdCl2 treatment but increased with 0.5 and 1 mM CdCl2 treatment in rice roots.96 Additionally, the relative abundance of most proteins, including sucrose synthase, gluconase proteasome subunit α type 6, ATP-binding cassette transporter and L-ascorbate peroxidase, decreased in a Cd-concentrationdependent manner, probably due to Cd toxicity.96 Most of the differentially abundant proteins belong to the antioxidative process (L-ascorbate peroxidase, peroxidase, and putative glutathione-S-transferase OsGSTU6), carbon metabolism (sucrose synthase, PGM, putative glyceraldehyde-3-phosphate dehydrogenase, and fructose-bisphosphate aldolase), chaperones (DnaK-type molecular chaperone hsp-70), and unknown proteins. Root and leaf proteomes showed significantly different patterns upon short-term Cd treatment. The relative abundance of GSH was dramatically decreased after Cd (100 μM for 24 h) treatment in roots, but no significant difference was observed in Cd-treated leaf tissues, suggesting the high toxicity of Cd in roots compared with leaves.94 More than half of the highly accumulated proteins (NADH-ubiquinone oxidoreductase,

Arsenic

Comparative proteomic study of rice roots in combination with physiological and biochemical analyses revealed that arsenic (As) induced As accumulation, lipid peroxidation, GSH, and H2O2 aggregation in rice roots.102 Twenty-three differentially abundant proteins containing SAMS, cysteine synthase (CS), and tyrosine-specific protein phosphatase protein were identified upon As treatment.102 Most of these identified proteins have a role in cell signaling (oxo-phytodienoic acid 4661



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studies provide information regarding rice responses to metal stress.93

reductase and SAM), stress and detoxification [GST, CS, arsenate reductase, chalcone synthase (CHS)-like, and putative tyrosine-specific protein phosphatase protein (TSPP)], defense and development [glucan endo-1,3-β-D-glucosidase, DUF26like protein, mannose-binding rice lectin, and salt-induced protein (SALT)], and protein biosynthesis (glutamine synthetase root isozyme).102 GSH activity responded to As in a dose-dependent manner, suggesting that it plays a central role in As tolerance.102 Differentially expressed proteins in rice leaves were found to be involved in energy production [formate dehydrogenase, NADP-dependent malic enzyme (NADPME)], carbon metabolism [glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and dihydrolipoamide dehydrogenase], secondary metabolism (carboxyvinyl-carboxyphosphonate phosphorylmutase, and putative r40c1 protein), and photosynthesis (chloroplast 29 kDa ribonucleoprotein and RuBisCO LSU).103 Most importantly, As stress in the rice leaf leads to reduced levels of the RuBisCO LSU, which may lead to decreased photosynthesis rates.103 As-responsive proteins in rice leaves were related to energy production, carbon metabolism, secondary metabolism, and photosynthesis (Figure 2E).

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RESPONSES OF RICE PROTEOME TO MINERALS Mineral nutrients are crucial for plant growth and development because most function as cofactors of several proteins and enzymes involved in energy production (mitochondrial electron transport chain) and metabolism. However, excess minerals in the soil can have deleterious effects on plant growth and development. Numerous proteomic analyses of the responses of rice to copper (Cu), aluminum (Al), manganese (Mn), and phosphorus (P) have been conducted. Copper

Copper (Cu) is an essential element in plants and plays diverse roles in biological electron transport and is a component of several proteins and enzymes. Cu plays a crucial role in several metabolic processes, photosynthesis, hormone regulation, and the oxidative stress response.107 However, excess Cu can be toxic to plants because high concentrations have inhibitory effects on normal growth and development.108,109 Several studies have been conducted on proteome profiling of Cu stress in rice.91,93,110−112 Cu stress significantly affects photosynthetic apparatus (RuBisCO LSU, SSU, and RuBisCO activase precursor fragment), oxidative process (SOD)j and defense-related proteins (OsPR5 and OsPR10) in rice leaves (Figure 2F).93 This suggests that Cu plays an important role in defense and photosynthesis in rice. Increased relative abundances of antioxidant and stressrelated proteins (glyoxylase I, peroxiredoxin, and aldose reductase) and regulatory proteins (DnaK-type molecular chaperone, UlpI protease, and receptor-like kinase) in germinating rice seeds under excess Cu suggest the possibility of establishment of new homeostasis to counterbalance Cu stress (Figure 2F).110 Reduced germination rates, shoot elongation, plant biomass, and water content were correlated with the decreased relative abundance of key metabolic enzymes, such as α-amylase or enolase, in germinating seeds.110 Furthermore, proteomic analysis of rice seed embryos under Cu stress revealed increased relative abundance of metallothionein-like proteins, membrane-associated proteins, putative wall-associated protein kinases, pathogenesis-related proteins, and the putative small GTP-binding protein Rab2.111 Decreased relative abundances of small cytochrome PY50 (CYP9002), a putative thioredoxin, and a putative GTPase were also identified.111 Antioxidative defense (putative peroxidase, L-ascorbate peroxidase 2, and cytosolic) redox regulation (thioredoxin-like 3−3 and putative glutaredoxin-C14), sulfur, and GSH metabolism [cysteine synthase (CS) and gamma-glutamyl cysteine synthase], carbohydrate metabolism (fructokinase-2), and signal transduction (serine/threonine protein kinase) processes are also affected by Cu stress in rice roots (Figure 2F).112 The Cu tolerance shown by the B1139 variety might be due to the significant increase in the relative abundance of putative CS, probable serine acetyltransferase 3, L-ascorbate peroxidase 1, putative glutathione S-transferase 2, and thioredoxin-like 3−3 compared with the Cu-sensitive variety B1195.112

Mercury

Mercury (Hg) and most of its compounds are extremely toxic and can easily penetrate cells and accumulate for long periods of time.104 Hg can induce oxidative damage in plants by means of excessive ROS generation, causing cell structure disruption and lipid peroxidation.105 However, little research has been conducted on the effect of Hg on rice proteome levels. Recently, Chen et al.106 reported the biochemical and proteomic changes in rice roots under Hg stress. Hg stress leads to reduced root growth rates with increased Hg content, ROS, and lipoxygenase activity in roots.106 Hg stress affects mainly redox and hormone homeostasis (ascorbate peroxidase), chaperone activity (protein disulfide isomerase-like), metabolism (enoyl-ACP reductase and malate dehydrogenase), transcription regulation (GCN5-related N-acetyltransferase), photosynthesis (RuBisCO LSU, RuBisCO activase precursor fragment, and photosystem II 23 kDa protein), and defenserelated proteins (OsPR5) (Figure 2E).93,106 Additionally, a rapid reduction in GSH was identified during Hg stress.106 Much proteomic research in rice under Hg stress remains to be conducted to fully understand the mechanism of Hg stress. Other Metals

Several other metals, such as cobalt (Co), zinc (Zn), strontium (Sr), and lithium (Li), are essential for plant growth and development if present at optimum concentrations in the soil. High soil concentrations of these metals have toxic effects on plants, inhibiting production and yield. Comparisons of the proteome patterns of rice leaves under various metal stresses were performed by Hajduch et al.93 providing information useful for the understanding of rice responses. OEE2 protein and the photosystem II 23 kDa protein were highly accumulated under Co, Zn, Sr, and Li stress in rice leaves.93 The relative abundance of the RuBisCO activase precursor fragment was increased by Li and Zn but remained unchanged by Co and Sr.93 Defense-related proteins (OsPR5 and OsPR10) were highly accumulated under Li and Zn.93 Hajduch et al.93 suggested that the photosynthetic process is affected by Co, Zn, Sr, and Li, whereas the defense system is affected by Li and Zn stress only. Additionally, photosynthesis-related proteins were not affected by Co and Sr treatment.93 These

Aluminum

Aluminum (Al) toxicity is the primary limiting factor in crop yields.113 To our knowledge, to date only two proteomic analyses have been performed on rice roots under Al stress.114,115 Proteomic analysis of the Al-resistant cultivar Xiangnuo 1 (XN1) 4662



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peroxiredoxins in NIL6−4 compared with Nipponbare under phosphorus deficiency suggest efficient ROS detoxification in NIL6−4 for tolerance of phosphorus deficiency.120

showed increased relative abundance of Cu−Zn SOD, GST, and SAM2 upon Al treatment.114 Most Al-responsive proteins are related to signal transduction (G protein β subunit-like protein) and antioxidation and detoxification (cysteine synthase, GST, SAMS, ACC oxidase, and SOD).114 Cysteine synthase might be a key player in rice Al tolerance based on the proteomic and metabolomic analyses of Yang et al.114 In Koshihikari, an Al-resistant cultivar, proteins involved in the antioxidant system [manganese superoxide dismutase (Mn-SOD) and glutathione S-transferase GST 30] and carbohydrate and nucleotide anabolism (phosphoenolpyruvate carboxylase, S-like ribonuclease, and nucleoside diphosphate kinase) were increased in relative abundance, whereas proteins involved in pathogenesis (pathogenesis-related protein PR-1a) and carbohydrate catabolism (aconitase, malic enzyme, pyruvate decarboxylase, and β-1,3-glucanase) were decreased in relative abundance in Kasalath, an Al-sensitive cultivar.115 Differential regulation of proteins involved in signal transduction, translation, and transcription differed between the two cultivars.115 In conclusion, proteins involved in the antioxidative system and carbohydrate metabolism might be involved in Al tolerance in rice (Figure 2F).

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PROTEOMICS OF RADIATION-INDUCED RESPONSES IN RICE

UV Radiation

UV radiation is a part of the electromagnetic (light) spectrum that reaches the earth from the sun.121,122 UV radiation can inhibit the growth of plants, including rice and maize, resulting in low yield.123−125 It was reported that UV radiation may induce plants to generate ROS and inhibit photosynthesisrelated proteins, such as Chl a/b-binding proteins, and induce defense-related proteins at the mRNA level.126,127 However, few proteomic analyses of rice under UV radiation have been conducted. Comparison of proteomic analyses between the UV-B tolerant Lemont cultivar and the UV-B-sensitive Dular cultivar showed significantly different protein patterns in leaves under UV-B radiation.128 The relative abundances of proteins involved in photosynthesis (RuBisCO binding-protein α-subunit, RuBisCO LSU and oxygen evolution complex protein 1), cell defense (4-coumarate coenzyme A ligase), protein metabolism (aminotransferase y4uB), signal transduction (tyrosine phosphatase), glycometabolism (inorganic pyrophosphatase), and lipid metabolism (delta 12 oleic acid desaturase) were increased in the Lemont cultivar, suggesting that accumulation of those proteins contributes to tolerance to UV-B exposure.128 However, all of the above-mentioned proteins were unchanged in the Dular cultivar.128 A study by Du et al.129 showed a slightly different differentially regulated proteome pattern than that reported by Wu et al.128 in which proteins involved in phytohormone synthesis (tryptophan synthase α chain and SAMs), detoxification/ antioxidation (glyoxalase I), RNA processing (glycine-rich protein), defense (Chitinase and Bet v I family protein), and secondary metabolism (isoprenoid biosynthesis-like protein) were altered in rice leaves by UV exposure (Figure 2G).128,129 The difference in proteome patterns between the two studies might be due to the different rice cultivars used for proteomic analysis, the growth stage of the rice, or the duration of UV exposure.128,129 Further detailed analyses of the effects of UV radiation on the rice proteome are necessary due to the increased level of UV radiation penetrating the atmosphere.

Manganese

Excess manganese (Mn) in soil inhibits growth and crop yields.116,117 Comparisons of the response to Mn in Mnsensitive and -tolerant crop species, such as wheat and barley, respectively, showed that elevated Mn supply increased Mn concentrations 30-fold in both bulk leaf and apoplastic washing fluid (AWF) without any symptoms in rice.118 However, Mn toxicity symptoms were shown by young rice leaves.118 Typical brown spots were seen on older barley leaves under low Mn concentrations in both bulk leaf and AWF, indicating severe Mn toxicity.118 Peroxidase activity was also drastically reduced in rice leaf AWF in comparison with barley, suggesting that peroxidase mediates apoplastic lesions in Mn toxicity.118 Furthermore, proteomics analysis revealed that proteins related to translational processes (chloroplast translational elongation factor Tu and 50S ribosomal protein L11) were most affected in old rice leaves, whereas increased abundances of putative inorganic pyrophosphate, adenosine 5′-phosphotransferase 2, and PBZ1 protein were identified in young leaves treated with excess Mn (Figure 2F).118 On the basis of their physiological and proteomic analyses, Fuhrs et al.118 suggested that the high Mn tolerance of old rice leaves is due to the high Mn-binding capacity of the cell walls and Mn toxicity in young leaves is due to Mn-induced Fe and Mg deficiencies.

Ozone

Ozone (O3), which is found in both the stratosphere and troposphere, has both protective and damaging effects. Stratospheric ozone protects the surface of the earth from harmful solar UV radiation. However, tropospheric ozone is a major phytotoxic air pollutant that severely damages plant tissue, resulting in decreased productivity and yield quality.130 Because of its strong oxidizing potential, ozone primarily affects plant photosynthetic tissues and generates ROS, causing severe oxidative damage and symptoms such as chlorosis, bronzing, and formation of necrotic lesions.131,132 At the proteome level, ozone causes severe damage to the photosynthesis mechanism, with a down regulation of photosynthetic proteins such as RuBisCO LSU and SSU, RuBisCO activase, and oxygen-evolving proteins, for example, OEE1 and OEE2, glycine dehydrogenase protein, and chloroplast ribonucleoprotein.4,10 The reduction in photosynthetic apparatus proteins correlates with visible necrotic damage to the leaves after ozone treatment.4,10 Oxidative stress is another mechanism of the damaging effect of ozone. Accumulation of APX, manganese

Phosphorus

Phosphorus (P) is one of the most important plant nutrients; its deficiency can be counterbalanced by use of phosphorus fertilizer.119 However, this is not economically practical, and excess phosphorus in the soil causes eutrophication.119 Few proteomic analyses of the response of rice to phosphorus have been conducted. Torabi et al.120 evaluated the effects of normal and deficient phosphorus levels in the roots of Nipponbare and NIL6−4, which possess a major phosphorus uptake QTL (Pup 1). Phosphorus deficiency significantly reduced root weight and tiller number in Nipponbare compared with NIL6−4.120 Phosphorus deficiency mainly affects proteins involved in oxidative stress (Cu− Zn SOD, GST, and 2-cys peroxiredoxins), the citric acid cycle (isocitrate dehydrogenase and aconitase), signal transduction (ASR1 protein), and plant defense responses (chitinases) as well as proteins with unknown functions (Figure 2F).120 Increases in the relative abundances of Cu−Zn SOD, GST, and 2-cys 4663



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superoxide dismutase (MnSOD), ascorbate peroxidase, and glutathione peroxidase in response to ozone stress indicates the essential role of these antioxidant enzymes in protecting plants from oxidative damage.4,10 Furthermore, proteins related to the regulation of redox status and protein folding, such as HSP90 and chloroplast HSP70, were also induced by ozone.4 Calcium-binding protein 1, calreticulin, ATP-dependent CLP protease, aconitate hydratase, fumarylacetoacetate hydrolase, C2-domain-containing protein, and thiamine biosynthetic enzyme were also differentially expressed in response to ozone treatment.4,10 Surprisingly, defense-related proteins including PBZ, PR10, PR5, and L-APX accumulated to high levels in response to ozone treatment. This indicates a defensive role for these proteins during ozone stress as well as providing evidence of a connection between ozone stress and pathogen responses.4,10 Ozone may function as an elicitor in the plant immune response.133 Further detailed analysis of the accumulation of defense-related proteins in response to ozone will provide a clearer picture of the link between ozone stress and defense responses to plant pathogens. Of the abiotic stresses, ozone stress has been least studied by proteomic techniques. Ozone stress gives rise to visible necrotic lesions on leaf surfaces, decreased rates of photosynthesis, and increased levels of antioxidant enzymes and defense-related proteins (Figure 2H).4,10

membranes under heat stress varies between plants. In rice, heat stress increased the relative ion leakage, whereas in poplar significant increase in ion permeability has been observed at higher temperature (higher than 45 °C).46,145 Furthermore, proteomics analysis of rice under ozone stress for 24 h (recovery time) identified rapid accumulation of defense proteins such as OsPR5, OsPR10s, APX, MnSOD, and an ATP-dependent CLP protease.10 Contrastingly, in poplar, PCA (principle component analysis) of protein abundant until 3 days of ozone treatment showed no significant difference between control and treated samples.146 However, at 35 days (recovery time), most of the proteins involved in photosynthesis (RuBisCO activase precursors) that decreased in abundance in poplar upon ozone stress returned to their initial level, suggesting the acclimation to the ozone stress.146 These observations suggest the differences in stress acclimation time for rice and poplar.10,146 Similarly, cadmium stress induced most of the proteins related to oxidative stress and GSH metabolism (GST, peroxidase, and APX1) in rice roots, whereas some of the oxidative stress-related proteins (Cu/Zn-SOD and peroxidase) were decreased in abundance in poplar.98,147 Thus, comparisons of differential proteome pattern between different plant species and different genotypes to a given stress could contribute to the identification of certain proteins responsible for the difference in tolerance or susceptibility.

COMPARATIVE PROTEOMICS ANALYSES IN DIFFERENT PLANT SYSTEMS Differentially abundant proteome patterns between different plant systems have common as well as strikingly different features. Under stressed condition, plants activate several defense mechanisms such as accumulation of ROS scavenging enzymes and other proteins with detoxification properties, chaperones for protein conformation that ultimately contribute to the plant stress acclimation with the establishment of new cellular homeostasis. Common features that are remarkably affected by various abiotic stresses in different plant systems are photosynthesis, carbon metabolism, antioxidation, and energy metabolism (Figure 2A−H). A decrease in relative abundance of putative aconitate hydratase was found in both rice and Arabidopsis upon cold stress, suggesting that cold stress altered TCA cycle in both species.7,134 As previously mentioned, cold stress induces degradation of photosynthesis-related proteins (RuBisCO LSU) in rice, and, similarly in pea, glycine dehydrogenase P protein was degraded by cold stress.7,135 Cold tolerance in maize and rice was related to the phosphorylation of RNA binding protein cp29.136,137 An increase in relative abundance of cp29 upon cold stress has also been reported in Arabidopsis and Thellungiella.138,139 Homologues of germin-like protein were found to decrease in relative abundance under heat stress in both rice and barley.54,140 An increase in abundance of UGPase activity under cold stress has also been reported in poplar similar as in rice.36,141 However, it is evident from the numerous previously and recently done studies that tolerance mechanisms to a given stress vary among different plant species or even different genotypes within one species.54,67,86,142 For example, HSP 70 was highly accumulated in Arabidopsis, pea, and winter wheat upon cold stress.29,135,143 In contrast with the above observation, HSP 70 was decreased in abundance in rice upon cold stress, implying that HSP70 might function differently in rice under cold stress.30 Heat-tolerant and -sensitive maize lines differentially regulate elongation factor Tu under heat stress, suggesting the correlation between heat tolerance and sensitivity.144 Thermostability of cell

CONCLUSIONS AND FUTURE PERSPECTIVES This review has been focused on the impact of various major abiotic stresses on the rice proteome, as determined by proteomics techniques such as 2D-PAGE coupled to LC-MS/MS. Extensive proteomics research has been conducted in many plant species, including maize, Arabidopsis, wheat, and rice. Here we reviewed the most recent information regarding the proteome of rice, one of the most widely consumed crops, in response to various abiotic stresses. Major differentially regulated proteins identified by proteomics analysis under various abiotic stresses are provided in the Supporting Information (Figure S1). A detailed summary of studies performed to date on the rice proteome under abiotic stress could result in a better understanding of the physiological mechanisms underlying the responses to different stresses and facilitate identification of the proteins involved in stress tolerance. This could enable elucidation of the protein−protein interactions that occur under various abiotic stress conditions and their physiological significance. Both unique and common rice proteome responses have been identified based on the type, severity, and duration of the given stress as well as plant growth stage and the organelle used for proteomic analysis. The most common rice proteome responses identified under all abiotic stresses include photosynthesis apparatus, redox homeostasis, detoxification/antioxidation pathway, carbohydrate metabolism, and protein metabolism (Figure 2A−H). However, some unique proteome responses are also identified such as vitamin B biosynthesis, histone modification, and vesicle trafficking under cold stress; caryopsis development under heat stress; cell structure under drought stress; membrane stabilization, GA signaling, and auxin/IAA pathway under salt stress; and thiamine biosynthesis under ozone stress (Figure 2A−H). Nevertheless, the comparative proteome analysis under various abiotic stress conditions on different plant systems would further enable us to understand the specific rice proteome responses as well as common responses among all other plant systems. Further characterization of key stress-tolerance proteins could provide biomarkers of stress responses. ROS production is common to all

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SAMS2, S-adenosylmethionine synthetase; TCA, tricarboxylic acid cycle; UGPase, UDP-glucose pyrophosphorylase; UV, ultraviolet

of the above-described responses to abiotic stresses. More attention should be paid to the proteomics of rice subcellular compartments (e.g., membranes, mitochondria, and nucleus). Specific attention should also be paid to the relationship between phosphoproteomics and abiotic stress signaling. This will provide further important information regarding the connections between individual stress-responsive proteins and the sophisticated abiotic stress signaling pathways. However, our understanding of the response of the rice proteome to abiotic stress needs to be further refined. Finally, the summary provided in this review will provide future direction by highlighting remaining questions regarding the role of the rice proteome in abiotic stress tolerance. This will ultimately enable us to refine and significantly improve the quality and productivity of rice for the benefit of humankind.

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(1) Tester, M.; Bacic, A. Abiotic stress tolerance in grasses. From model plants to crop plants. Plant Physiol. 2005, 137, 791−793. (2) Boyer, J. S. Plant productivity and environment. Science 1982, 218, 443−448. (3) Folgado, R.; Panis, B.; Sergeant, K.; Renaut, J.; Swennen, R.; Hausman, J. F. Differential Protein Expression in Response to Abiotic Stress in Two Potato Species: Solanum commersonii Dun and Solanum tuberosum L. Int. J. Mol. Sci. 2013, 14, 4912−4933. (4) Cho, K.; Shibato, J.; Agrawal, G. K.; Jung, Y. H.; Kubo, A.; Jwa, N. S.; Tamogami, S.; Satoh, K.; Kikuchi, S.; Higashi, T.; Kimura, S.; Saji, H.; Tanaka, Y.; Iwahashi, H.; Masuo, Y.; Rakwal, R. Integrated transcriptomics, proteomics, and metabolomics analyses to survey ozone responses in the leaves of rice seedling. J. Proteome Res. 2008, 7, 2980−2998. (5) Bohnert, H. J.; Gong, Q.; Li, P.; Ma, S. Unraveling abiotic stress tolerance mechanisms–getting genomics going. Curr. Opin. Plant Biol. 2006, 9, 180−188. (6) Gygi, S. P.; Rochon, Y.; Franza, B. R.; Aebersold, R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 1999, 19, 1720−1730. (7) Yan, S. P.; Zhang, Q. Y.; Tang, Z. C.; Su, W. A.; Sun, W. N. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol. Cell. Proteomics 2006, 5, 484−496. (8) Pradet-Balade, B.; Boulmé, F.; Beug, H.; Müllner, E. W.; GarciaSanz, J. A. Translation control: bridging the gap between genomics and proteomics? Trends Biochem. Sci. 2001, 26, 225−229. (9) Potters, G.; Pasternak, T. P.; Guisez, Y.; Palme, K. J.; Jansen, M. A. Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci. 2007, 12, 98−105. (10) Agrawal, G. K.; Rakwal, R.; Yonekura, M.; Kubo, A.; Saji, H. Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (Oryza sativa L.) seedlings. Proteomics 2002, 2, 947−959. (11) Agrawal, G. K.; Rakwal, R. Rice proteomics: A move toward expanded proteome coverage to comparative and functional proteomics uncovers the mysteries of rice and plant biology. Proteomics 2011, 11, 1630−1649. (12) Agrawal, G. K.; Jwa, N. S.; Rakwal, R. Rice proteomics: ending phase I and the beginning of phase II. Proteomics 2009, 9, 935−963. (13) Chen, S.; Harmon, A. C. Advances in plant proteomics. Proteomics 2006, 6, 5504−5516. (14) Lafitte, H. R.; Ismail, A.; Bennett, J. Abiotic Stress Tolerance in Rice for Asia: Progress and the Future. Proceedings of the 4th International Crop Science Congress, 26 Sep−1 Oct 2004, Brisbane, Australia. (15) Singh, R.; Lee, M. O.; Lee, J. E.; Choi, J.; Par, J. H.; Kim, E. H.; Yoo, R. H.; Cho, J. I.; Jeon, J. S.; Rakwal, R.; Agrawal, G. K.; Moon, J. S.; Jwa, N. S. Rice mitogen-activated protein kinase interactome analysis using the yeast two-hybrid system. Plant Physiol. 2012, 160, 477−487. (16) Seo, Y. S.; Chern, M.; Bartley, L. E.; Han, M.; Jung, K. H.; Lee, I.; Walia, H.; Richter, T.; Xu, X.; Cao, P.; Bai, W.; Ramanan, R.; Amonpant, F.; Arul, L.; Canlas, P. E.; Ruan, R.; Park, C. J.; Chen, X.; Hwang, S.; Jeon, J. S.; Ronald, P. C. Towards establishment of a rice stress response interactome. PLoS Genet. 2011, 7, e1002020. (17) Wankhede, D. P; Misra, M.; Singh, P.; Sinha, A. K. Rice mitogen activated protein kinase kinase and mitogen activated protein kinase interaction network revealed by in-silico docking and yeast two-hybrid approaches. PLoS One 2013, 8, e65011. (18) Ding, X.; Richter, T.; Chen, M.; Fujii, H.; Seo, Y. S.; Xie, M.; Zheng, X.; Kanrar, S.; Stevenson, R. A.; Dardick, C.; Li, Y.; Jiang, H.; Zhang, Y.; Yu, F.; Bartley, L. E.; Chern, M.; Bart, R.; Chen, X.; Zhu, L.; Farmerie, W. G.; Gribskov, M.; Zhu, J. K.; Fromm, M. E.; Ronald, P.

ASSOCIATED CONTENT

S Supporting Information *

Summary of differential proteome analysis under major abiotic stress responses. Major high abundant and low abundant proteins in each stress factors are shown. For references, see Table 1. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +82-02-3408-3645. Fax: +82-02-3408-4336. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center; No. PJ008061), Rural Development Administration, Republic of Korea, and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (grant number: 2013R1A1A2009269). We appreciate S. Dangol for the artwork of the rice plant in Figure 1. We apologize to those researchers whose publications have not been cited owing to space limitations.

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ABBREVIATIONS ALT, alanine aminotransferase; ATP, adenosine triphosphate; ABC transporter, ATP-binding cassette transporters; 2DE, twodimensional electrophoresis; ABA, abscisic acid; APX, ascorbate peroxidase; CPK1, calcium-dependent protein kinase 1; GCMS, gas chromatography mass spectrometry; GSH, glutathione; GST, glutathione S-transferase; HSP, heat shock protein; IAA, indole-3-acetic acid; LEA, late embryogenesis abundant; LCMS/MS, liquid chromatography tandam mass spectrometry; MnSOD, magnesium superoxide dismutase; MALDI-TOF/ TOF, matrix-assisted laser desorption/ionization time-of-flight; NADP, nicotinamide adenine dinucleotide phosphate; Nramp, Natural resistance-associated macrophage proteins; OEE2, oxygen-evolving enhancer 2; PSII, photosystem II; PRK, phosphoribulokinase; PR, pathogen related; PR 10, pathogenesis-related 10; PR 5, pathogenesis-related 5; PBZ, probenazole-inducible protein; PGM, phosphoglucomutase; RuBisCO, ribulose-1,5-bisphosphate carboxylase oxygenase; SOD, superoxide dismutase; sHSP, small heat shock protein; 4665



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