Plant Cell Organelle Proteomics in Response to Abiotic Stress

REVIEWS pubs.acs.org/jpr

Plant Cell Organelle Proteomics in Response to Abiotic Stress Zahed Hossain,†,‡ Mohammad-Zaman Nouri,†,§ and Setsuko Komatsu*,† †

National Institute of Crop Science, Tsukuba 305-8518, Japan Department of Botany, West Bengal State University, Kolkata-700126, West Bengal, India § Rice Research Institute of Iran, Deputy of Mazandaran, Amol 46191-91951, Iran ‡

bS Supporting Information ABSTRACT:

Proteomics is one of the finest molecular techniques extensively being used for the study of protein profiling of a given plant species experiencing stressed conditions. Plants respond to a stress by alteration in the pattern of protein expression, either by up-regulating of the existing protein pool or by the synthesizing novel proteins primarily associated with plants antioxidative defense mechanism. Improved protein extraction protocols and advance techniques for identification of novel proteins have been standardized in different plant species at both cellular and whole plant level for better understanding of abiotic stress sensing and intracellular stress signal transduction mechanisms. In contrast, an in-depth proteome study of subcellular organelles could generate much detail information about the intrinsic mechanism of stress response as it correlates the possible relationship between the protein abundance and plant stress tolerance. Although a wealth of reviews devoted to plant proteomics are available, review articles dedicated to plant cell organelle proteins response under abiotic stress are very scanty. In the present review, an attempt has been made to summarize all significant contributions related to abiotic stresses and their impacts on organelle proteomes for better understanding of plants abiotic stress tolerance mechanism at protein level. This review will not only provide new insights into the plants stress response mechanisms, which are necessary for future development of genetically engineered stress tolerant crop plants for the benefit of humankind, but will also highlight the importance of studying changes in protein abundance within the cell organelles in response to abiotic stress. KEYWORDS: cell organelle, plant proteomics, abiotic stress

’ INTRODUCTION Abiotic stress is the major constraint that global crop production faces at present. New techniques have been adopted to dissect the underlying molecular mechanisms of plants’ stress sensing and tolerance. When a plant encounters abiotic stress, for example, salinity, drought, flooding, metal toxicity, UV exposure, high and low temperature, the fine cellular adjustment between the formation of reactive oxygen species (ROS) and the quenching capacity of plants’ antioxidant molecules get distorted. The excess ROS produced under abiotic stress leads to oxidative damages to lipids, proteins and nucleic acids (Figure 1).1,2 To cope with the stress, plants have evolved complex antioxidant defense mechanism comprised of both enzymatic and nonenzymatic networks. r 2011 American Chemical Society

The cellular mechanism of sensing stress and transduction of stress signals into the cell organelle is of well-known and represents the initial reaction of plant cells toward stress.3 Stress signals are first encountered by the outer part of the cell and the process for sensing environmental changes and activating the responsive mechanism is highly organized.4 The ROS which are chiefly formed by the over reduced electron transport chain during abiotic stress, are recognized as a signal to activate the plant defense response.5 Transduction of the signal into the cell Special Issue: Microbial and Plant Proteomics Received: August 31, 2011 Published: October 26, 2011 37

dx.doi.org/10.1021/pr200863r | J. Proteome Res. 2012, 11, 37–48

Journal of Proteome Research

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during the stressed condition represent the primary defense response. In fact, communication between organelles and cytosolic, luminal proteins renders the protein composition of organelles dynamic.6 Most of the receptor proteins are located in the plasma membrane, and thus the cell membrane is directly involved in sensing stress.7 To obtain a comprehensive understanding about the cellular reactions involved in cell defense mechanisms, the role of cellular organelles should be considered in stress-related studies. Proteomics, the cutting edge molecular technique of the present time, offers several advantages over the genome-based technologies as it directly deals with the functional molecules rather than genetic code or mRNA abundance. Identification of proteins using mass spectrometry has opened a new avenue for organ and subcellular proteome research. Organelle proteome analysis provides fundamental information of plant response to a given stress at the functional level and thus refines our knowledge about plant stress related signaling pathways. A plethora of reviews on proteome analysis in plant stress research are available (Supplementary Table 1, Supporting Information), but review articles specifically devoted to changes in the organelle proteome under abiotic stresses are really scant. The present review provides an overview of the current major findings related to changes in organelle proteomes in response to abiotic stresses for better understanding of the abiotic stress tolerance mechanism of plants at the protein level.

’ ORGANELLE PROTEOME Analyses of an organelle’s proteins are useful approach to understand the cell behavior under abiotic stress conditions. Organelle proteins are primarily nuclear-encoded, but some organelles, such as mitochondria and chloroplasts, carry their own genetic material that enables them to synthesize proteins themselves.6 However, because of the dynamic state of organelles and their proteins, elucidating the subcellular distribution and expression of organelle proteins has always been a challenging job for proteomic researcher.8 Abiotic stress alters interactions between organelles in plant cells, and this subsequently changes the regulation and secretion of proteins in cellular organelles and compartments. Several secretory pathways have been reported to be involved in targeting proteins in plant cells.9,10 Signal peptides play a central role in protein targeting, and several amino acid residues and protein domains involved in specific targeting have been successfully determined.11 Recent studies reveal that golgito-plastid trafficking of certain chloroplast resident proteins involve glycosylation before entering the chloroplast. Posttranslational modifications like N-glycosylation and intramolecular disulfide bridge formation are important determining factors for correct protein folding and trafficking of target proteins from secretory pathway to chloroplast.12 15 Thus, identifying organelle proteins involved in the stress response, especially those with regulatory or protein targeting functions would definitely enhance the knowledge of the cellular stress response. A number of proteomics studies have been successfully carried out on specific cellular organelles and compartments in plants subjected to abiotic stresses (Table 1), including the mitochondria,16 20 nucleus,21 23 chloroplasts,24 26 cell wall,27 30 and the plasma membrane.31 33 However, the literatures lack critical discussion of the role played by cooperation between organelles responding to abiotic stress. This review highlights the current state of plant cell organelle proteome in response to abiotic stress.

Figure 1. Abiotic stress-induced ROS/antioxidant imbalance and its cellular impact. Abbreviations: ROS, reactive oxygen species; O2•‑, superoxide radical; H2O2, Hydrogen peroxide; 1O2, singlet oxygen; OH•, Hydroxyl radical; SOD, superoxide dismutase; APX, ascorbate peroxidase; MDAR, monodehydroascorbate reductase; DHAR, dehydroascorbate reductase; GR, glutathione reductase; GSH, reduced glutathione; AsA, reduced ascorbate.

through cascades alters gene and protein expression levels, leading to physiological responses. Hence, communication through intracellular compartments plays a crucial role in stress signal transduction process. To understand the underlying molecular mechanism of how a plant cell modulates its protein expression network to cope with the stress, an in-depth study of the organelle proteome is of great contribution toward development of stresstolerant crop varieties to meet the increasing demand of food supply worldwide. The major subcellular organelles, whose functions get affected under abiotic stress, are the nucleus, mitochondria, chloroplasts, peroxisomes, plasma membrane and cell wall. Most of these organelles have the potential to become a source of ROS. The intracellular organelles and compartments and their interactions 38

dx.doi.org/10.1021/pr200863r |J. Proteome Res. 2012, 11, 37–48

39

a

Nucleus

Nucleus

Nucleus

Chloroplast

Chloroplast

Rice

Chickpea

Arabidopsis

Soybean

Arabidopsis

Plasma

Soybean

membrane

Plasma

membrane

Plasma

Cold

Osmotic stress

Flooding

Dehydration

Water deficit

Flooding

Dehydration

Ozone

Low temperature

Ozone

Cold

Dehydration

Dehydration

Salinity

and herbicide

Drought, cold

Oxidative stress

Salinity

Flooding

abiotic stress

IP, Number of identified proteins.

Arabidopsis

Soybean

ECM/Cell wall

Chickpea

membrane

Cell wall

Maize

Cell wall

Mitochondria

Rice

Soybean

Mitochondria

Pea

Cell wall

Mitochondria

Arabidopsis

Rice

Mitochondria

Wheat

Chloroplast

Mitochondria

Soybean

Poplar

organelle

plant

2-DE/MALDI TOF MS

2-DE/nanoLC MS/MS

nanoLC MS/MS

2-DE/MALDI TOF MS

2-DE/LC TOF MS

2-DE/Q-TOF MS

nanoLC MS/MS

2-DE/MALDI TOF MS

2-DE/LC TOF MS

2-DE/MALDI TOF MS

MALDI TOF MS

2-DE/

2-DE/MALDI TOF MS

2-DE/MALDI TOF MS

2-DE/LC TOF MS

2-DE/LC ESI MS/MS

2-DE/MALDI TOF MS

38

86

14 + 8 = 22

134

152

16

94

27

43

32

184

147

109

8

29

Q-TOF MS

164

LC ESI MS/MS 2DE, BN-PAGE,

68

36 + 16 = 52

IPa

SDS-PAGE/

2-DE/LC MS/MS

MALDI TOF MS

2-DE/BN-PAGE/

methods

major findings

26

25

24

23

22

21

19

20

18

17

16

ref.

osmotic stress, enhancement of CO2 fixation and proteolysis.

Cold responsive proteins are mainly associated with membrane repair, protection of the membrane against

because of up-regulation of plasma membrane H1-ATPase protein.

Under hyperosmotic conditions, calnexin accumulates in the plasma membrane and high ion efflux takes place

and degradation.

up-regulated in plasma membrane; heat shock cognate proteins protect stress induced protein denaturation

Flooding stress induced proteins mostly involved in antioxidative defense system. Cell wall proteins found to be

More than hundred ECM proteins with a variety of cellular functions e.g. cell wall modification, signal transduction, metabolism, and cell defense and rescue, play crucial roles in dehydration stress sensing and tolerance mechanism.

about the complex mechanisms regulating root growth under water stress.

the apical region of the elongation zone of water stressed maize roots and hence provides novel information

Water stress-responsive proteins were identified and categorized, into 5 groups; apoplastic ROS level increases in

lignifications suppressed under flooding stress.

Two lipoxygenases, germin-like protein precursors, glycoprotein precursors, SOD down-regulated and

cell defense and rescue, cell wall modification, cell signaling and molecular chaperones.

33

32

31

30

29

28

stress, leading to a decrease in abundance of photosystem subunits and other proteins of the chloroplast membranes. Dehydration-responsive proteins mainly involved in a variety of functions, including carbohydrate metabolism, 27

Under a long-term ozone exposure, the cellular protective measures get exhausted by the oxidative nature of the

stress sensing and signal transduction, presumably helping the plant in cold sensing and acclimatization.

biosynthesis and

Identified proteins chiefly participate in photosynthesis, other plastid metabolic functions, phytohormone

Proteins involved in antioxidant defense and carbon metabolism increased under O3 stress.

pathways and cross-talk.

Proteins with cold stress response-specific motifs/functions detected, mainly involved in RNA-associated functions, elongation step of protein synthesis, prevents protein misfolding, suggesting involvement of multiple signaling

molecular chaperones, cell signaling, and chromatin remodeling.

Differentially expressed proteins apparently involved in functions related to gene transcription and replication,

remodeling, signaling, gene regulation, cell defense and rescue, and protein degradation.

Dehydration responsive proteins involved in variety of functions e.g. transcriptional regulation and chromatin

ATP synthase may not be the major producer of ATP in mitochondria during the early stage of PCD in rice.

proteins indicates the diversity of response of mitochondria to stresses at the protein level.

metal affinity and varying susceptibility of inactivation by metal ions. Differential degradation of key matrix enzymes, induction of heat shock proteins and specific losses of other

Metal content of mitochondria is dynamic and changes during oxidative stress. Different proteins have varying

varieties at whole plant level.

Differences in mitochondrial ROS scavenging pathways determine the salinity tolerance of the contrasting wheat

cycle and γ-amino butyrate shunt were up-regulated.

Flooding stress directly impairs electron transport chains, significantly decreased ATP; proteins related to TCA

Table 1. Summary of Published Organelle Proteome Analyses in Response to Abiotic Stress

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metal ions. Mitochondrial respiratory chain pathways and the matrix enzymes varied widely in terms of their susceptibility toward metal-induced loss of function and thus exhibiting the selective oxidation events in the mitochondrial proteome. In-depth study of mitochondrial proteome during salt stressinduced programmed cell death (PCD) in rice was performed by Chen et al.19 A total of eight PCD-related proteins were identified after 2-DE analysis. Out of them, four proteins were up-regulated after PCD induction, which are glycoside hydrolase, mitochondrial heat shock protein 70, 20S proteasome subunit, and Cu/Zn-SOD, and rest four were down-regulated, namely ATP synthase beta subunit, cytochrome-c oxidase subunit 6b, S-adenosylmethionine synthetase 2, and transcription initiation factor eIF-3 epsilon. Proteome study reveals that ATP synthase may not be the major producer of ATP in mitochondria during the early stage of PCD in rice. Glycoside hydrolase could be involved in ETC impairment and ROS burst during salt stress-induced PCD. Taylor et al.20 analyzed the response of pea mitochondria under drought, cold and herbicide stresses. Mitochondria isolated from the stressed pea plants maintained their electron transport chain activity, but changes were apparent in the abundance of uncoupling proteins, nonphosphorylating respiratory pathways, and oxidative modification of lipoic acid moieties on mitochondrial proteins. Meticulous analysis of the soluble proteins of mitochondria by 2D-PAGE and MS reveals differential degradation of key matrix enzymes under chilling and drought stresses. In addition, differential induction of heat shock proteins and specific losses of other proteins indicates the diversity of response of mitochondria to these abiotic stresses at the protein level.

Mitochondrial Proteome

Study of mitochondrial proteome has revealed new insights of plants response toward abiotic stress factors. In addition of acting as a cellular power house, mitochondria also performs numerous other activities like nucleotide and vitamins synthesis, lipids and amino acids metabolisms, involvement in the photorespiratory pathway.34 Under stress, the mitochondrial electron transport chain become over reduced, favoring the generation of O2•‑ thus affecting plant growth and development.35 Kruft et al.36 first used the two-dimensional polyacrylamide gel electrophoresis (2-DE) technique to study the mitochondrial proteins. Thereafter, much attention has been paid to separate proteins for analyzing plant mitochondrial proteome under stressful condition. Gel-free method of mitochondrial proteome study using nanoscale 1D and 2D liquid chromatography (LC) offers advantages37 39 over the gel-based techniques, as it allows separation of highly acidic or highly basic proteins, very high and very low molecular weight proteins as well as low-abundance proteins. Mitochondria have been a target for subcellular proteomic study, as most of the abiotic stresses primarily impair mitochondrial electron transport chain resulting excess ROS generation. A comprehensive analysis of mitochondrial proteins of roots and hypocotyls of soybean under flooding stress has recently been performed.16 Mitochondrial matrix and membrane proteins were separated by 2-DE and blue native-polyacrylamide gel electrophoresis (BN-PAGE), respectively. Differentially expressed proteins and metabolites were identified using MS. Proteins and metabolites related to the tricarboxylic acid cycle (TCA) and γ-amino butyrate shunt were increased by flooding stress, while inner membrane carrier proteins and proteins related to complexes III, IV, and V of the electron transport chains were decreased. The authors found that the amounts of NADH and NAD were increased; however, ATP was significantly decreased under flooding stress. The results led them conclude that flooding stress directly impairs electron transport chains, although NADH production increases in the mitochondria through the TCA cycle. The shoot mitochondrial proteome and differences associated with salinity tolerance have been extensively investigated in two contrasting salinity tolerant and sensitive wheat cultivars.17 By employing reference map and 2D-fluorescence difference gel electrophoresis (DIGE) technique, they identified five mitochondrial proteins, whose abundance changed under salinity treatment. These proteins include Mn- SOD, nucleoside diphosphate kinase, cysteine synthase, voltage dependent anion carrier and alternative oxidase (AOX). Both Mn-SOD and AOX play pivotal role in scavenging ROS that are produced in excess under salinity stress.40 The authors suggested that the differences in the mitochondrial ROS defense pathways observed in the mitochondrial proteomes of the two contrasting cultivars play key role in salinity tolerance at whole plant level. Heavy metals have known functions of depleting cellular glutathione pools, thus causing an impairment of ascorbate glutathione cycle resulting higher accumulation of ROS in the cell compartments.41 Inhibition of plant mitochondrial function under Cd-stress has been reported earlier.42,43 Tan et al.18 investigated the metal homeostasis in Arabidopsis mitochondria during oxidative stress for better understanding of protein interactions with metal ions and the associated modulation of protein functions in plant mitochondria. Their findings demonstrated that the metal content of mitochondria is dynamic and changes during oxidative stress and the different proteins have varying metal affinity and varying susceptibility of inactivation by

Nuclear Proteome

Nucleus carries the information necessary for controlled expression of proteins and thus plays essential role in determining plant response toward abiotic stress. Like the other organelle proteomic study, nuclear proteome has recently gained importance, as identification of novel nuclear proteins help us better understand protein function in conferring cellular stress tolerance. Limited information on the proteomic study of stress responsive nuclear protein expression profile in plants is currently available. A comprehensive nuclear proteome analysis was carried out in rice for better understanding of molecular mechanisms governing dehydration-responsive adaptation.21 Organellar enrichment followed by 2-DE based protein identification by LC electrospray ionization tandem mass spectrometry (ESI MS/MS) techniques were exploited for proteome determination. The differential display of nuclear proteome revealed 150 protein spots whose intensities changed significantly during dehydration period. A total of 109 differentially regulated proteins were identified and expected to be involved in a variety of functions including transcriptional regulation and chromatin remodeling, signaling and gene regulation, cell defense and rescue, and protein degradation. A similar kind of dehydration responsive nuclear proteome study was performed in chickpea, providing information about the complex metabolic network operating in the nucleus during dehydration.22 Under stress, 205 protein spots were found to be differentially regulated. Following MS analysis, 147 differentially expressed proteins were identified, apparently involved in functions related to gene transcription and replication, molecular chaperones, cell signaling, and chromatin remodeling. The dehydration responsive nuclear proteome of chickpea revealed a coordinated response, which involves both the regulatory as well as the functional proteins. Comparison 40



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between the dehydration responsive nuclear proteome of rice and chickpea revealed a crop-specific adaptation mechanism with some common resident proteins. Response to cold stress and changes in nuclear protein expressions were thoroughly investigated in model plant Arabidopsis.23 Nuclear proteins were isolated and peptide masses were measured using 2-DE and matrix-assisted laser desorption/ionization timeof-flight (MALDI-TOF) MS respectively. Out of the total 184 identified proteins, 54 were up- or down-regulated by more than a factor of 2 in response to cold stress. In addition, proteins with defined stress response-specific motifs or functions were also detected. The function of protein motifs in conferring abiotic stress tolerance has been well studied in Arabidopsis.44,45 The EARmotif of the Cys2/His2-type zinc finger proteins was found to be responsible in enhancing tolerance to cold, drought and salinity stressed conditions. The ZPT2-related proteins primarily function as transcriptional repressors that down-regulate the trans-activation activity of other transcription factors.

directly or indirectly by ozone exposure. Findings indicate that under a long-term ozone exposure, the cellular protective measures get exhausted by the oxidative nature of the stress, leading to a decrease in abundance of photosystem subunits and other proteins of the chloroplast membranes. Taking all into considerations, more initiatives must be taken to characterize chloroplast proteome for more comprehensive understanding of chloroplast’s functional biology in response to abiotic stress. Cell Wall Proteome

Plant cell wall plays essential role in stress sensing and signal transduction between the apoplast and symplast. Hence, in recent years cell wall proteome science has been the subject of intense research. For better understanding of the underlying molecular mechanism of dehydration stress response in rice seedlings, Pandey et al.27 studied the stress-induced changes in the extracellular matrix proteins proteome by using two-dimensional gel electrophoresis. The proteomic analysis led to identification of about 100 differentially expresses proteins, which might play key roles in plants’ dehydration tolerance cascade. Investigation on the function of the soybean cell wall revealed that 16 out of 204 cell wall proteins responded to flooding stress.28 Of these, two lipoxygenases, four germin-like protein precursors, three stem glycoprotein precursors, and one Cu Zn SOD were reported to be down-regulated. Proteome analysis suggested that the roots and hypocotyls of soybean caused the suppression of lignification through decrease of the proteins by down-regulation of reactive oxygen species and jasmonate biosynthesis under flooding stress. To achieve a comprehensive understanding of alterations in the cell wall protein composition of different regions of the maize root elongation zone to water deficit, a proteomics approach was initiated to examine water-soluble and loosely ionically bound cell wall proteins.29 The results revealed region-specific changes in protein profiles among control and water-stressed roots. All together, 152 water stress-responsive proteins were identified and categorized into five groups based on their functions in the cell wall ROS metabolism, defense and detoxification, hydrolases, carbohydrate metabolism, and other/unknown. Protein identification reveals that the apoplastic ROS level increases in the apical region of the elongation zone of water stressed maize roots and hence provides novel information about the complex mechanisms regulating root growth under water stress. Comprehensive extracellular matrix proteome analysis of chickpea under dehydration stress was performed by Bhushan et al.30 The comparative proteomics study led to the identification of 134 differentially expressed proteins, which include predicted and some novel dehydration-responsive proteins. This comparative proteomics study demonstrates that more than 100 extracellular matrix proteins with a variety of cellular functions like cell wall modification, signal transduction, metabolism, and cell defense and rescue play crucial roles in dehydration stress sensing and tolerance mechanism. Compared to mitochondrial proteomics, only few researches so far have been carried out on cell wall proteomics. Still, quite a large number of cell wall proteins remain unidentified. Hence, there is an urgent need to investigate the functional proteomics of cell wall proteins under abiotic stress.

Chloroplast Proteome

Environmental stresses like salinity, drought, ozone and high or low temperatures cause reduction in CO2 fixation; thus, NADP+ regeneration by the Calvin cycle get decreased. As a consequence, the photosynthetic electron transport chain becomes over reduced, forming superoxide radicals and singlet oxygen in the chloroplasts.46 Excess ROS impairs chloroplast protein functions involved in photosynthesis. Only few works so far been carried out on the chloroplast proteome response to abiotic stress. Proteome analysis of soybean chloroplasts responding to ozone stress by Ahsan et al.24 revealed 32 differentially expressed chloroplast proteins. Proteins involved in photosystem I/II and carbon assimilation decreased under stress, and this might be one of the reasons of reduced photosynthetic activity in response to ozone. In contrast, proteins involved in antioxidant defense and carbon metabolism increased under stress. The authors came to the conclusion that not only do the degradation of starch and higher amounts of sucrose in response to short-term acute ozone exposure feed the TCA cycle but the availability of sucrose may also play a pivotal role in oxidative stress signaling and regulation pathways of antioxidative processes.47,48 Subcellular fractionation and relative protein quantification by 2D-DIGE technique were used to get the insights of the Arabidopsis chloroplast proteome response to short-term cold shock and long-term cold acclimation.25 Cold shock resulted in minimal change in the plastid proteomes, while short-term acclimation caused major changes in the stromal but few changes in the lumen proteome. In contrast, long-term acclimation resulted in modulation of the proteomes of both compartments, with appearance of new proteins in the lumen and further changes in protein abundance in the stroma. In total, 43 differentially displayed proteins were identified that participate in photosynthesis, other plastid metabolic functions, phytohormone biosynthesis and stress sensing and signal transduction, presumably helping the plant in cold sensing and acclimatization. Ozone exposure is known to cause chloroplasts to become smaller and distortion of thylakoids shape and structure.49,50 Effects of ozone stress on the chloroplast membrane proteins was analyzed using 2D-DIGE.26 Extrinsic photosystem proteins and ATPase subunits were found to vary in abundance. A decrease trend in protein abundance was observed under stress, except for ferredoxin-NADP+ oxidoreductase. This led to the formation of higher NADPH, which helps in detoxification of ROS generated

Plasma Membrane Proteome

At the cellular level, the plasma membrane is probably the most diverse form of membrane with a complex protein composition 41



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Table 2. Classification of Major Defense-related Abiotic Stress Responsive Proteins and Their Subcellular Localization protein group Osmoprotectant regulators

proteins Sucrose synthase, sugar transporter

abiotic stress

subcellular localization

Drought, Osmotic stress

Nucleus, mitochondria, chloroplast, endoplasmic reticulum, Golgi apparatus, plasma membrane, cell wall

ROS scavengers

Superoxide dismutase, ascorbate peroxidase, monodehydroascorbate

Ion transporters

Salinity, Flooding, Drought,

Nucleus, mitochondria, chloroplast,

Chilling, Heat, Radiation stress

peroxisomes, vacuole, endoplasmic

reductase, dehydroascorbate reductase,

reticulum, Golgi apparatus, plasma

glutathione reductase, glutathione

membrane, cell wall

peroxidase, catalase Na+/H+ antiporters, plasma membrane

Salinity, Osmotic stress

Plasma membrane, Tonoplast

H+-ATPase Water channels

Aquaporins

Drought, Flooding,

Plasma membrane, Tonoplast

Molecular chaperones

HSPs, calnexin, calreticulin, binding

Drought, Heat, Ozone,

Nucleus, mitochondria, chloroplast,

immunoglobulin protein

Osmotic stress, Heavy metal stress

vacuole, endoplasmic reticulum Golgi apparatus, plasma membrane, cell wall

Proteolysis-related proteins

Ubiquitins

Drought, Salinity

that varies with cell types, developmental stages and environments.51 It acts as a primary interface between the cellular cytoplasm and the extracellular environment, thus playing a vital role in cell communication. Change in gene expression at the protein level is one of the main cellular responses required for perception of a stress signal and its transduction into the cell, which mostly happens in the plasma membrane. To explore the alterations in the plasma membrane proteins of soybean exposed to flooding stress, small purified plasma membrane proteins were analyzed using gel-based and gel-free proteomics techniques.31 It is presumed to be the first report of identifying flood induced plasma membrane proteins in soybean exploring 2-DE MS/sequencer-based proteomics and nanoLC MS/MS-based proteomics techniques. A total of 35 stress induced novel proteins were identified, mostly involved in plants’ antioxidative defense system. Nouri and Komatsu32 investigated the polyethylene glycol induced osmotic stress impact on plasma membrane proteome of soybean. Plasma membranes were purified using a two-phase partitioning method and their purity was verified by measuring ATPase activity. Using the gel-based proteomics, four and eight protein spots were identified as up- and down regulated respectively, whereas in the nanoLC MS/MS approach, 11 and 75 proteins were identified as up- and down-regulated respectively under polyethylene glycol treatment. Osmotic stress responsive proteins, for example, transporter proteins and proteins with high number of transmembrane helices as well as low-abundance proteins were identified by the gel free proteomics. Three homologues of plasma membrane H+-ATPase, the transporter proteins involved in ion efflux, were up-regulated under osmotic stress. Among the identified proteins, seven proteins were mutual in two proteomics techniques, in which calnexin was the highly up-regulated protein. Findings suggested that under hyperosmotic conditions, calnexin accumulates in the plasma membrane and high ion efflux takes place because of up-regulation of plasma membrane H+-ATPase protein. Mass spectrometric approach was widely used for identification of putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation.33 A significant change in protein profile was observed after cold acclimation. A total of 38 proteins

Cytoplasm, endoplasmic reticulum, nucleus

were identified using MALDI-TOF MS. The proteins that changed in quantity during the first day of cold acclimation include those, which are mainly associated with membrane repair, protection of the membrane against osmotic stress, enhancement of CO2 fixation and proteolysis. Plasma membrane proteomics study describes the functional machinery of membrane proteins and thus considered to be a core area of investigation in the field of developmental plant proteomics. All the above-mentioned researches would not only provide the functional information of individual protein, but also throw light on the protective role of plasma membrane proteins in response to stress. Organelle proteome study provides valuable information about protein functions, interactions and sorting mechanisms; however, limitations in individual organelle isolation, purification and analysis of low abundance proteins make the task extremely difficult for studying abiotic stress tolerance mechanism in endomembrane organelles.52

’ STRESS-RESPONSIVE PROTEINS IN PLANT CELL ORGANELLES Exposure of plant cells to abiotic stress leads to a wide range of changes in protein expression level. Any change in the accumulation of a particular protein in the cell does not necessarily mean that gene expression has also increased or suppressed, as there is no certain correlation between gene expression and the final product of protein synthesis and regulation. Protein expression can be affected by a number of factors, such as protein targeting or translocation and post-translational modifications, all of which are influenced by stress conditions. Secretory pathways and intracellular interactions affect the distribution of proteins in the cell. Groups of functionally related proteins are often regulated as a result of exposure to abiotic stress. Some of these proteins, such as those related to metabolism, storage, and protein synthesis, are not directly involved in the mechanism of defense. Defense-related abiotic stress-responsive proteins can be classified into six major groups according to their functions (Table 2). Osmoprotectant Regulators

Osmoprotectant regulators are proteins that regulate the distribution of osmolyte molecules such as sugar, mannitol, or 42



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amino acids (proline) and their N-methyl derivatives (betaines). The solutes increase the osmotic pressure in the cell, thereby preventing further water loss and maintaining turgor.53 Studies on plants’ response against abiotic stress have revealed that expression of genes for sugar synthases and sugar transporters are usually up-regulated under abiotic stress54 and that accumulation of proline55 and glycinebetaine56 helps the plants to overcome the stressed condition, thus enhancing the tolerance capacity. Osmoprotectants are found in the cytoplasm and all organelles except for the vacuoles.53 The osmoprotectant biosynthetic protein Δ1-pyrroline-5-carboxylate synthase as well as other enzymes such as sucrose synthase and sugar transporters have been identified in soybean undergoing osmotic stress and stress affecting the endoplasmic reticulum.57 Adjustment of osmotic potential is one of the initial reactions of plant cells to dehydration-related stresses. Osmoprotectants and water channels are usually responsible for preserving the water content of cells under stress conditions.

enzymes; therefore, proper regulation of ion efflux is vital during stress conditions. Water Channels

Adjustment of water content is necessary for plant cells, and it is critical when plants are undergoing abiotic stress. Since water is involved in many cellular processes, any change in the water content of the cell can negatively affect the proper functioning of the cell. Aquaporins are water channel proteins that reside in the plasma membrane and vacuoles and facilitate the diffusion of water and small neutral solutes across the cell membrane.70,71 Aquaporins are divided into two main classes according to their localization in the cell and sequence homology: plasma membrane-intrinsic aquaporins, and tonoplast-intrinsic aquaporins. The tonoplast has high water permeability; therefore, the vacuolar space can play a buffering role under osmotic fluctuations.72 The activity of aquaporins is regulated by phosphorylation under drought stress. In the case of stresses associated with an excess of water, such as flooding or submergence, the cytoplasmic pH falls, leading to protonation of the conserved residue of aquaporin. This process subsequently leads to closure of water channels in the plasma membrane.73 Water-related stress constitutes the most frequent and significant environmental factor affecting plants, and water channel proteins in the tonoplast and plasma membrane are the primary regulators of water balance in plant cells. Adjustment of the water content in the cell upon exposure to water-related stress enables the cell to maintain proper function of proteins and enzymes in the organelles and other cellular compartments.

ROS Scavengers

Cells undergoing abiotic stress transiently produce various ROS, such as hydrogen peroxide, hydroxyl radicals, and superoxide anions, all of which in turn cause oxidative stress. The cell’s stress response depends on the severity of the oxidative stress, and may range from activation of antioxidant defense mechanisms to programmed cell death. The production of ROS scavenger proteins is the primary defense against the oxidative stress. The major scavenger proteins found in plant cells are superoxide dismutase, ascorbate peroxidase, glutathione peroxidase, and catalase.58 60 The production of ROS in organelles such as the mitochondria and chloroplasts is a normal cellular process. However, stress conditions accelerate the production of ROS and cause oxidative damage.61 The presence of scavenger proteins during abiotic stress has been reported in various plant organelles and subcellular compartments, including the nucleus,23 mitochondria,62 chloroplasts,63 plasma membrane,31 and cell wall.64 The distribution of scavenger proteins throughout the cell suggests that ROS may serve as signaling molecules in the organelles and compartments.

Molecular Chaperones

The primary function of molecular chaperones is facilitating the folding of proteins through binding to newly synthesized glycoproteins. The chaperone proteins assist in the proper folding and assembly of secretory proteins74 and they are normally present in almost all parts of a cell. However, the majority of chaperone proteins are found in the endoplasmic reticulum, where newly synthesized proteins are folded. Calnexin, calreticulin, binding immunoglobulin protein, and most of the heat shock proteins belong to this group.75 Expression of molecular chaperone proteins prevents protein aggregation and helps the cell to adapt the unfavorable environmental conditions.76 Several investigations have confirmed changes in the regulation of chaperone proteins in response to abiotic stress.31,76,77 The expression of molecular chaperones does not follow a set of pattern in response to stress. The age of the plant and the severity and duration of the stress could influence whether a given protein would be up-regulated or downregulated. Furthermore, the expression of a molecular chaperone can vary across organelles. For these reasons, studies on the molecular chaperone subproteome must be carefully planned with respect to the stress conditions and type of cells and organelles involved.

Ion Transporters

Changes in the flux of H+, K+, Cl , and Ca2+ ions across the plasma membrane alters the cytosolic pH and transmembrane electrical potential. Sun et al.65 reported that accumulation of these ions in plant tissues could induce stress. The concentrations of Na+ and Cl ions are normally kept low in plant cells, while nutritionally important elements such as K+ are maintained at high concentrations. Salinity is a typical abiotic stress that may upset the homeostasis of Na+, H+, K+, and Cl ions. The plasma membrane and vacuoles are the two major subcellular components of cells that are involved in maintaining ion balance.65,66 Regulator proteins, such as tonoplast Na+/H+ antiporters and plasma membrane Na+/H+ antiporters, play important roles in sequestering Na+ in vacuoles or extruding it to the external environment, respectively.67,68 Proton pumps associated with the plasma membrane facilitate stomatal closure under drought stress by mediating the efflux of K+ and various anions from guard cells. In this process, Ca2+ regulates the activity of plasma membrane H+-ATPase.69 Plasma membrane proton pumps are the integral membrane proteins that are involved in maintaining the ion balance of the cell under osmotic stresses. Homeostasis of intracellular ions is important for the activity of many cellular

Proteolysis-Related Proteins

Misfolded, unassembled, or mutated proteins are degraded in cells through a proteolytic process. The endoplasmic reticulum, which is the major site of protein folding and quality control, also has a specific proteolytic system. The protein breakdown mechanism is usually mediated by ubiquitin, although proteolysis without ubiquitin is possible.78 It was reported that the ubiquitinproteasome system of the endoplasmic reticulum degradation machinery also extends into the cytoplasm.79 The protein 43



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Figure 2. Classification of abiotic stress-related proteins and their subcellular distributions. Negative effects of abiotic stress regulate 6 major groups of defense-related proteins. Examples of proteins are represented in the parentheses and the main locations of the proteins are represented in brackets. All, all cellular organelles, compartments and cytoplasm; PM, plasma membrane; Ton., tonoplast; ER, endoplasmic reticulum; Cyto., cytoplasm.

consequence of water deficit is enhanced H2O2 production.81 Interestingly, ABA itself stimulates H2O2 production by the membrane bound enzyme NADPH oxidase,82,83 which basically catalyzes the production of another free radical superoxide from oxygen and NADPH.84 However, recent findings suggest that water stress-induced ABA actually prevents the excessive accumulation of H2O2, by inducing CATB gene expression.85 In the plant cell, H2O2 acts as a signaling molecule and activates mitogen-activated protein kinase (MAPK) cascade for stress responsive genes expression.84,86 Nuclear proteome analyses lead to the identification of stress signal transduction pathway components like serine/threonine protein kinase, histidine kinase, tyrosine phosphatase.21,22 In addition, presence of FCA protein (a known nuclear ABA receptor87) suggests its involvement in the ABA signaling pathway. Transcription factors (TFs) are the key proteins that facilitate the transcription process. Several TFs like RF2b, bZIP, HB3, homeobox-leucine zipper protein were found to be up-regulated under dehydration stress.21,22 Basically, early stress response genes are activated first, producing TFs for induction of delayed stress response genes.88 The superoxide radicals formed as a result of NADPH oxidase activity need to be scavenged quickly to protect the nucleus from oxidative damage to DNA. SOD acts as the first level of defense against ROS as it directly controls the concentrations of two important ROS namely superoxide radicals and hydrogen peroxide. The excess H2O2 in turn gets nutralized by the activity of APX or GPX. Drought-induced up-regulation of SOD, APX, GPX, GST proteins21,22 suggests the presence of well-equipped antioxidant system in plant nucleus to cope with the abiotic stresses. Apart from antioxidants, accumulation of molecular chaperons (HSP20, HSP70, Chap60, dnaK) helps in refolding of misfolded proteins. In addition, drought induced synthesis of DHNs proteins further give protection to the membrane from stress induced damages.89,90 Mitochondria and chloroplasts are the two potential subcellular sites for ROS generation. Under water deficit condition, electron transport chains get overreduced resulting formation of superoxide radicals and singlet oxygen. Mitochondrial proteome study reveals the abundance of

degradation pathways of the ubiquitin-proteasome have also been found in nucleus.21 Since abiotic stress leads to the accumulation of misfolded and unfolded proteins, protein breakdown and recycling is an essential feature of the plant response to environmental stress.80 Proteolytic proteins and molecular chaperones represent two groups of stress-responsive proteins that directly interact with target proteins. The activity of proteolysisrelated proteins can be considered as the last step in the cell’s effort to survive under stress conditions. Organelles are specified to operate cellular functions in cooperation with other compartments. Role of each organelle individually or in combination with cytosol or other compartments is described. Abiotic stress has wide range of deleterious effects on the cell and the survival of plant cell under stress condition highly depends on the interaction among organelles and compartments. The major negative effects of abiotic stress can be classified into 4 categories including changes in osmotic potential or water content, ROS production, ion imbalance and protein misfolding or aggregation (Figure 2).

’ MODULATION OF ORGANELLE PROTEOME UNDER DROUGHT STRESS Plant experiences drought stress when there is a shortage of water around the root zone. Among the different abiotic stress factors, drought is the most adverse environmental condition that negatively affects plant growth, development and yield throughout the world. Different aspects of plant response toward dehydration stress are well documented. However, sufficient information on drought sensing and tolerance mechanism at the organelle proteome level is not available. In this section, published proteomic works on dehydration stress mediated changes in organelle proteomes are summerized for better understanding of the stress responsive signal pathway and functional role of defense related proteins in conferring stress tolerance at organelle level (Figure 3). Transient increase in endogenous ABA level in response to drought stress triggers the downstream response that eventually leads to expression of stress responsive genes. Another inevitable 44



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Figure 3. Drought stress induced activation of defense related organelle proteins. The scheme is based on the published proteomic works on dehydration stress mediated changes in organelle proteomes.20 22,26,29 Abbreviations: ABA, abscisic acid; H2O2, hydrogen peroxide; NADP, Nicotinamide adenine dinucleotide phosphate; SOD, superoxide dismutase; APX, ascorbate peroxidase; GPX, glutathione peroxidase; HSPs, heat shock proteins; Ser/Thr, serine-threonine; His, histidine; DHNs, dehydrins; ROS, reactive oxygen species; O2.‑, superoxide radical; TF, transcription factor.

Cu Zn isoform of SOD in drought stressed pea mitochondria.20 Up-regulation of antioxidant enzymes (APX, SOD, MDAR) in cell wall27,30 further confirms the presence of a robust antioxidative defense system at the organelle level. In addition, abundance of chaperonin in mitochondrial as well as in cell wall proteomes20,27,30 ensures proper protein folding under dehydration stress. Survey of articles on organelle proteomics under abiotic stress has revealed that not much information is available on droughtmediated changes in the chloroplast proteome. In addition, a large number of stress-induced organelle proteins remain unidentified. So, there is an urgent need of initiating organelle proteomic research particularly in chloroplast to dissect the stress responsive proteins in conferring plant stress tolerance.

mechanisms. In-depth analysis of the research works done in recent times revealed that proteome researcher mainly used 2-DE technique to separate the protein pool while studying the plant abiotic stress response at organelle level. Interestingly, both 2-DE/MALDI-TOF MS and gel free-LC MS/MS systems were extensively used for identification of differentially expressed organelle proteins under stress. To understand the mechanism of stress tolerance, a detailed study of membrane proteins is important as they play key role in stress signal perception and transduction to turn-on the stress responsive genes. As most of the organelle membrane proteins are hydrophobic in nature, nanoLC MS/MS gel free system would be the most promising technique for identification of such proteins. By summerizing significant contributions related to abiotic stresses and organelle proteomes, efforts have been made in the review to delineate the molecular basis of acquisition of stress tolerance mechanism at the organelle level. This would further enable us to find proteinbiomarkers linked to plants’ abiotic stress tolerance. Instead of applying the finest proteomics techniques, many organelle proteins either stress-induced or house-keeping still remain unclassified. Future initiatives should be taken to identify and characterize those organelle proteins, which might open a new avenue for the proteome-based abiotic stress research. Finally,

’ CONCLUDING REMARKS The present review outlines the impact of various abiotic stressors on the plant cell organelle proteome. Improved protein extraction protocols and advance techniques for identification of novel proteins have been standardized in different plant species at both cellular and whole plant levels for better understanding of abiotic stress sensing and intracellular stress signal transduction 45



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we do hope that this review would not only provide new insights into the plants stress response mechanisms, which are necessary for future development of genetically engineered stress tolerant crop plants for the benefit of humankind, but would also highlight the importance of studying changes in protein abundance within the cell organelles in response to abiotic stress.

Jolivet, P.; Doonan, J. H.; Rakwal, R. Plant organelle proteomics: Collaborating for optimal cell function. Mass Spectrom. Rev. 2011, 30, 772–853. (7) Komatsu, S.; Konishi, H.; Hashimoto, M. The proteomics of plant cell membranes. J. Exp. Bot. 2007, 58, 103–112. (8) Boisvert, F. M.; Lam, Y. W.; Lamont, D.; Lamond, A. I. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 2010, 9, 457–470. (9) Furman, M. H.; Loureiro, J.; Ploegh, H. L.; Tortorella, D. Ubiquitinylation of the cytosolic domain of a type I membrane protein is not required to initiate its dislocation from the endoplasmic reticulum. J. Biol. Chem. 2003, 278, 34804–34811. (10) Mitoma, J.; Ito, A. The carboxy-terminal 10 amino acid residues of cytochrome b5 are necessary for its targeting to the endoplasmic reticulum. EMBO J. 1992, 11, 4197–4203. (11) Carter, C.; Pan, S.; Zouhar, J.; Avila, E. L.; Girke, T.; Raikhel, N. V. The vegetative vacuole proteome of arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 2004, 16, 3285–3303. (12) Buren, S.; Ortega-Villasante, C.; Blanco-Rivero, A.; MartínezBernardini, A.; Shutova, T.; Shevela, D.; Messinger, J.; Bako, L.; Villarejo, A.; Samuelsson, G. Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana. PLoS One 2011, 6 (6), e21021. (13) Kitajima, A.; Asatsuma, S.; Okada, H.; Hamada, Y.; Kaneko, K.; Nanjo, Y.; Kawagoe, Y.; Toyooka, K.; Matsuoka, K.; Takeuchi, M.; Nakano, A.; Mitsui, T. The rice alpha-amylase glycoprotein is targeted from the golgi apparatus through the secretory pathway to the plastids. Plant Cell 2009, 21 (9), 2844–2858. (14) Nanjo, Y.; Hiromasa, O.; Ikarashi, N.; Kaneko, K.; Kitajima, A.; Mitsui, T.; Jose Munoz, F.; Rodrıguez-Lopez, M.; Baroja-Fernandez, E.; Pozueta-Romero, J. Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 2006, 18, 2582–2592. (15) Villarejo, A.; Buren, S.; Larsson, S.; Dejardin, A.; Monne, M.; Rudhe, C.; Karlsson, J.; Jansson, S.; Lerouge, P.; Rolland, N.; von Heijne, G.; Grebe, M.; Bako, L.; Samuelsson, G. Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 2005, 7 (12), 1224–1231. (16) Komatsu, S.; Yamamoto, A.; Nakamura, T.; Nouri, M. Z.; Nanjo, Y.; Nishizawa, K.; Furukawa, K. Comprehensive analysis of mitochondria in roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. J. Proteome Res. 2011, 10 (9), 3993–4004. (17) Jacoby, R. P.; Millar, A. H.; Taylor, N. L. Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J. Proteome Res. 2010, 9, 6595–6604. (18) Tan, Y. F.; O’Toole, N.; Taylor, N. L.; Millar, A. H. Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol. 2010, 152, 747–761. (19) Chen, X.; Wang, Y.; Li, J.; Jiang, A.; Cheng, Y.; Zhang, W. Mitochondrial proteome during salt stress-induced programmed cell death in rice. Plant Physiol. Biochem. 2009, 47 (5), 407–415. (20) Taylor, N. L.; Heazlewood, J. L.; Day, D. A.; Millar, A. H. Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell. Proteomics 2005, 4 (8), 1122–1133. (21) Choudhary, M. K.; Basu, D.; Datta, A.; Chakraborty, N.; Chakraborty, S. 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. (22) Pandey, A.; Chakraborty, S.; Datta, A.; Chakraborty, N. Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol. Cell. Proteomics 2008, 7, 88–107. (23) Bae, M. S.; Cho, E. J.; Choi, E.-Y.; Park, O. K. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 2003, 36 (5), 652–663.

’ ASSOCIATED CONTENT

bS

Supporting Information Supplementary Table 1. A summary of published review articles on plant proteomics (2007 2011). This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Setsuko Komatsu, National Institute of Crop Science, Kannondai 2-1-18, Tsukuba 305-8518, Japan. Tel: +81-298-38-8693. Fax: +81-298-38-8694. E-mail: skomatsu@affrc.go.jp.

’ ACKNOWLEDGMENT Z.H. thankfully acknowledges the financial support provided through the DST-BOYSCAST fellowship programme, government of India for conducting advance research at National Institute of Crop Science, Japan. M.-Z.N. was supported by Monbukagakusho (Japanese government) scholarship program. This work was supported by the grants from National Agriculture and Food Research Organization, Japan. ’ ABBREVIATIONS: 2-DE, two-dimensional polyacrylamide gel electrophoresis; SDSPAGE, sodium dodecyl sulfate polyacrylamide gel electrophoresis; BN-PAGE, blue native-polyacrylamide gel electrophoresis; MS, mass spectrometry; MALDI TOF, matrix-assisted laser desorption ionization time-of-flight; Q-Tof, quadrupole time of fligh; LC ESI MS/ MS, liquid chromatography electrospray ionization tandem mass spectrometry; ROS, reactive oxygen species; TCA, tricarboxylic acid cycle; SOD, superoxide dismutases; AOX, alternative oxidase; PCD, programmed cell death; 2D-DIGE, two-dimensional fluorescence difference gel electrophoresis; MudPIT, multidimensional protein identification technology ’ REFERENCES (1) Halliwell, B.; Gutteridge, J. M. C. Free Radicals in Biology and Medicine; Oxford University Press: Oxford, U.K., 1999. (2) 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 (14), 3781–3801. (3) Desikan, R.; Hancock, J.; Neill, S. Oxidative stress signalling. In Plant Responses to Abiotic Stress. Topics in Current Genetics; Hirt, H., Shinozaki, K., Eds.; Springer-Verlag: New York, 2003; Vol. 4, pp 121 150. (4) Heino, P.; Tapio Palva, E. Signal transduction in plant cold acclimation. In Plant Responses to Abiotic Stress. Topics in Current Genetics; Hirt, H., Shinozaki, K., Eds.; Springer-Verlag: New York, 2003; Vol. 4, pp 151 186. (5) Vranova, E.; Atichartpongkul, S.; Villarroel, R.; Van Montagu, M.; Inze, D.; Van Camp, W. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (16), 10870–10875. (6) Agrawal, G. K.; Bourguignon, J.; Rolland, N.; Ephritikhine, G.; Ferro, M.; Jaquinod, M.; Alexiou, K. G.; Chardot, T.; Chakraborty, N.; 46



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Plant Cell Organelle Proteomics in Response to Abiotic Stress

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