Legume proteomics: Progress, prospects, and challenges

310 DOI 10.1002/pmic.201500257 Proteomics 2016, 16, 310–327 REVIEW Legume proteomics: Progress, prospects, and challenges Divya Rathi∗ , Dipak Gay...
Author: Russell Waters
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DOI 10.1002/pmic.201500257

Proteomics 2016, 16, 310–327

REVIEW

Legume proteomics: Progress, prospects, and challenges Divya Rathi∗ , Dipak Gayen∗ , Saurabh Gayali, Subhra Chakraborty∗∗ and Niranjan Chakraborty National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India

Legumes are the major sources of food and fodder with strong commercial relevance, and are essential components of agricultural ecosystems owing to their ability to carry out endosymbiotic nitrogen fixation. In recent years, legumes have become one of the major choices of plant research. The legume proteomics is currently represented by more than 100 reference maps and an equal number of stress-responsive proteomes. Among the 48 legumes in the protein databases, most proteomic studies have been accomplished in two model legumes, soybean, and barrel medic. This review highlights recent contributions in the field of legume proteomics to comprehend the defence and regulatory mechanisms during development and adaptation to climatic changes. Here, we attempted to provide a concise overview of the progress in legume proteomics and discuss future developments in three broad perspectives: (i) proteome of organs/tissues; (ii) subcellular compartments; and (iii) spatiotemporal changes in response to stress. Such data mining may aid in discovering potential biomarkers for plant growth, in general, apart from essential components involved in stress tolerance. The prospect of integrating proteome data with genome information from legumes will provide exciting opportunities for plant biologists to achieve long-term goals of crop improvement and sustainable agriculture.

Received: June 29, 2015 Revised: September 19, 2015 Accepted: November 5, 2015

Keywords: Crop improvement / Legumes / Nitrogen fixation / Plant proteomics / ROS detoxification / Stress response

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Additional supporting information may be found in the online version of this article at the publisher’s web-site

Introduction

Legumes contribute 27% of the world’s primary crop production and are a key to sustainable agriculture [1]. They constitute the third largest family with 946 genera and 24 505 accepted species (www.theplantlist.org). They are the indispensable part of human diet as they provide one-thirds of the dietary protein, while also serving as an important source of fodder and forage for animals, and of edible and industrial oils [2]. Legumes that possess root nodules contribute to symbiCorrespondence: Dr. Niranjan Chakraborty, National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi 110067, India E-mail: [email protected] Fax: 00-91-11-26716658 Abbreviations: ABA, abscisic acid; ECM, extracellular matrix; LEA, late embryogenesis abundant; NF, Nod factor; PBM, peribacteroid membrane; PR, pathogenesis related; RAM, root apical meristem; SNF, symbiotic nitrogen fixation

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otic nitrogen fixation (SNF) wherein mutualistic interactions with rhizobia are observed. This intimacy is explained by the fact that the former are estimated to be 60-million-year-old (myo), while the latter is 58 myo [3]. The cool season legumes that include bean, lentil, lupin, pea, chickpea, and grasspea are staple foods, whereas the warm season legumes such as soybean and peanut are oil crops, the former also being staple food in some parts of the world [4]. Molecular investigations in legumes have proceeded at an exponential pace at the genomic level, but not so at the proteomic level. Legumes that have been sequenced and assembled include Vigna radiata (mung bean), Arachis ipaensis, A. duranensis (groundnut), Trifolium pratense (red clover), Lupinus angustifolius (blue lupin), Cicer arietinum (chickpea), Phaseolus vulgaris (common bean), Medicago ∗ These

authors contributed equally to this work. corresponding author: Dr. Subhra Chakraborty E-mail: [email protected]

∗∗ Additional

Colour Online: See the article online to view Fig. 2 in colour.

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Figure 1. (A) Graphical representation of the number of protein sequences available in NCBI for all the legume genera (as tabulated in Supporting Information Table 1). The X-axis represents the number of protein sequences in logarithmic scale and the Y-axis represents the legumes. Asterisk (* ) represents those genera in which a single species name was used for search to remove nonspecific results [Lens*, Lotus*, and Glycine* correspond to Lens culinaris, Lotus japonicus, and Glycine max, respectively]. (B) A comparative account of the number of publications in representative legume genera (as tabulated in Supporting Information Table 1) generated using Pubmed on May 31, 2015. The keywords used during the search were “plant” and “proteom.*” The X-axis represents the number of publications and the Y-axis represents the legumes.

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truncatula (barrel medic), and Glycine max (soybean) (www.ncbi.org/genome), the latter being the first crop legume to be sequenced completely. As far as the online protein repository goes, the maximum number of sequences is that of soybean, followed by common bean and barrel medic (Fig. 1). Nonetheless, this number is far behind than that of Arabidopsis. Plant proteomics, the global analysis of the proteome, is important because it aims to assemble the entire repertoire of proteins, which can decode the molecular mysteries of plant survival. The major challenges that proteomics faces can be exemplified by the fact that many genes code for multiple proteins and those proteins undergo variety of PTMs. It is known that strong gene expression might coincide with the abundance of mRNA but not protein. Nevertheless, proteomic research is growing at a rapid rate focusing on protein quantity, PTMs, subcellular localization, and protein– protein interactions. Proteomic studies are higher in number in model plants and those with sequenced genomes [5]. Insights from the model legume species, barrel medic, could undoubtedly boost legume research, but it is not a crop and will never be suffice for the world population. Consequently, there is a great need for proteomic investigations of crop legumes. However, to be able to analyze such legumes particularly the orphan species, one must take several hindrances. Our recent survey on PubMed as of May 31, 2015 indicates that legume proteome research is still far behind in the plant proteomics field. The keywords “plant” and “proteom*” displayed 3828 publications and the keywords for all the legume genera (Supporting Information Table 1) and “proteom*” totalled to 393 publications. The representative legume genera with maximum number of publications are Medicago, Glycine, and Pisum (Fig. 1). Roughly, 90% of the legume proteomics has been accomplished through gel-based methods, especially 2DE. This highlights the command of 2DE in proteomics owing to its capability in separation and visualization of thousands of proteins, amenability to automation, and sensitivity. The acute shortcomings of 2DE, such as relatively low throughput, difficulty in resolving membrane proteins, and proteins of extreme pI, are customarily covered up by gel-free methods. Environmental stress and changing niches result in decreased yield of the primary food crops. In the past decades, barrel medic, and trefoil have emerged as model legumes to investigate the genetics of stress tolerance. The advantages these legumes offer are small diploid genomes, autogamous nature, short-generation times, prolific seed production [6], and higher degree of synteny [7]. Environmental stresses adversely affect plant growth and development besides reducing SNF rate [8, 9]. Such stresses include heat/chilling, dark, water-deficit/flooding, ozone exposure, UV-B irradiation, hypersalinity, heavy metal toxicity, and mineral deficiency. Legumes are majorly inflicted by fungal pathogens albeit insects, nematodes, viruses, bacteria, and parasitic weeds also drastically decrease the productivity. Therefore, stress-responsive studies might aid in legume improvement  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

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when coupled with marker-assisted breeding, in vitro mutagenesis and genetic transformation. This review highlights the major achievements in legume proteomics research as illustrated in Fig. 2. We discuss the proteomics at organ level in the first section, and organelle level in the second section. The third section focuses on proteomics-aided understanding of the stress responses in legumes. This orthoproteomic study may aid in comprehension of the complex mechanism of development and stress acclimation not only in legumes, but also in other crop species.

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Organ/tissue

The high-abundance of individual proteins or protein clusters in any organ is indicative of their organ specificity, implying their unique but distinct functions [10]. Whereas roots and seeds are the most extensively studied organs in legumes (Fig. 3, Supporting Information Fig. 1 and Supporting Information Table 2), these studies are limited by intrinsic complexities, such as, low protein yield and high levels of interference due to pigments and phenolic compounds. Since high-abundant proteins tend to mask the low-abundant ones, major attention needs to be focused on the improvement of protein extraction methods to develop high-resolution organbased proteome maps.

2.1 Meristem Plant apical meristems are established during embryogenesis and they serve as a source of stem cells for organogenesis and architectural integrity. The root apical meristem (RAM) produces all the tissues of the main root by a highly defined pattern of cell divisions. Proteomic analysis of soybean RAM revealed 342 proteins, of which 73 were overrepresented and primarily involved with the pathways for protein synthesis and processing, cell redox homeostasis, and flavonoid biosynthesis [11]. Proteins underrepresented in the root apex are those of glycolysis, tricarboxylic acid metabolism, and stress response [11]. An analysis of small proteins in root tips of barrel medic displayed an abundance of basic histone and ribosomal proteins, seed-specific storage proteins, late embryogenesis abundant (LEA), and lipid transfer proteins [12]. LEA proteins are associated with water-deficit as well as conditions of water limitation that arise during different developmental phases [13]. Proteomic analysis of meristematic tissues of barrel medic revealed an overaccumulation of proteins involved in cell division and redox processes, besides accumulation of pathogenesis related (PR) proteins [14].

2.2 Root As indicated above, root is the most extensively studied organ as against other organs owing to the dynamism in protein www.proteomics-journal.com

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Figure 2. Diagrammatic illustration of key aspects in legume proteomes (A) at the organ level and stress-responsive studies (B) organellar level and (C) method/s of investigation. Most of the legume proteomics has been accomplished with 2DE in contrast to the non-gel based proteomics.

profiles. Proteomic insights into general infection-specific responses of the nodule organogenesis and metabolic changes during SNF have greatly increased our understanding of rhizobial symbiosis. Over the past years, the root proteome maps have been established for barrel medic [10, 15–17],  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

trefoil [18,19], soybean [11,20–22], and lupin [23]. Rhizobiuminfection-specific maps have also been developed in barrel medic [24–30], soybean [31, 32], and common bean [33]. Legumes establish symbiotic interactions with nitrogenfixing bacteria as well as mycorrhizal fungi. Although the

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Figure 3. Figure showing status of publication in accordance to various legume species. The data used to build this chart corresponds to studies related to (A) organ-specific, (B) organelle-specific, and (C) stress-responsive proteomics. A colorful and dynamic view can be obtained at www.cicertransdb.esy.es/nipgr/legume_proteomics_graph.html.

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structures formed to support these interactions are different (nodules compared with arbuscules), there is conservation in early signaling between these two symbioses [34]. Calcium spiking is one of the earliest detectable plant responses to Nod factors (NF). Pharmacological studies have indicated the requirement for calcium channels and calcium ATPase in NF-induced calcium spiking. The roles of some proteins, such as CCaMK, GRAS, and the putative NF receptor, apparently fit well with the previous knowledge of this signaling pathway. The most notable proteins associated with nodulation and root development are metabolic enzymes, for instance, nodulins [15], ENOD16, and ENOD8 [10], besides ascorbate metabolic enzymes, and putative rhizobial effectors [19]. The other members are related to cell defense and rescue, metabolism, and transport [35, 36]. The positive evidence for coregulation of nodule formation by rhizobia and auxin has been established in roots of barrel medic [26]. Proteins induced in early phase of symbiotic interaction in legumes are not thoroughly explored. In vivo study of phosphorylation in barrel medic revealed NUP133, IPD3, and SKL as the early signaling proteins, whereas late signaling components included sucrose synthase 1, an alkaline invertase and a RNA-binding protein [37]. Dam et al. suggested that the number of PTMs is higher in nodule proteins as compared to that in nonnodulated roots [19]. Interestingly, the regulation of protein function through oxidative modification such as sulfenylation and phosphorylation emerged as an important molecular mechanism modulating nodulation [37–40]. Grimsrud et al. reported 3457 unique phosphopeptides spanning 3404 nonredundant sites of phosphorylation on 829 proteins in roots of barrel medic. Several of the phosphorylation motifs, including LxKxxs and RxxSxxxs, are yet to be reported as kinase. Multiple sites of phosphorylation were identified on several key proteins involved in initiating rhizobial symbiosis [37–40]. Time-dependent analysis of barrel medic symbiotic root proteome upon infection with Glomus mosseae revealed induction of 14 proteins at the arbuscular mycorrhiza appresorial stage (4 dpi) and 24 proteins at the symbiosis stage (3–4 weeks postinfection). These proteins are predominantly involved in defense response, cell wall modification, and root physiology [17]. Root hair (RH) is a terminally differentiated single cell type, mainly involved in water and nutrient uptake from the soil and plays a crucial role in symbiosis. These cells are attractive models owing to their ease of isolation, polar growth, and indispensable roles in plant growth [41]. Brechenmacher et al. identified 5702 proteins related to RH formation in soybean including proteins involved in nutrient uptake or vesicular trafficking [42]. Additionally, there have been attempts to establish initial rhizobia-RH infection and the underlying kinase cascades. The phosphoproteome of RHs and the corresponding stripped roots during rhizobial colonization provided new insights into the molecular mechanism of RH cell biology [32]. This study established that a significant number of proteins undergo phosphorylation in response to inocu C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

lation with B. japonicum [32]. Proteomic analysis of soybean roots inflicted with B. japonicum revealed that most differentially expressed proteins are associated with RHs, but not with primary root [43]. 2.3 Leaf and stem Approximately 40% leaf proteins are related to photosynthesis [10, 12, 18, 44]. This predominance of photosynthesis-related proteins is accounted by the Rubisco large (26.1%) and small subunit (2.8%), Rubisco activase (3.2%), and oxygen-evolving protein (6.4%). Besides proteins associated with photosynthesis and metabolism, proteins involved with signal transduction and transport systems are bona fide constituents of leaf proteome [10, 45–48]. Leaf proteome is significantly altered during intercropping events such that there is upregulation of proteins involved in photosynthesis, nutrient availability, and defense [49]. Stem proteome appears to be similar to that of leaf, albeit in low-abundance [10]. However, proteins involved in secondary metabolism are found in high-abundance in stem as against leaves. The alfalfa stem proteome when analyzed regionally (apical, intermediate, and basal) revealed several kinases and RNA-binding proteins, besides multiple ribosomal proteins. The pertinent findings were the profusion of chloroplast and mitochondrial-related proteins along with the abundance of proteins involved in the early steps of fiber production. However, forisomes and stress-related proteins were differentially accumulated in the mature basal region [50]. 2.4 Flower Proteins involved in energy metabolism, protein synthesis, and targeting dominate the flower proteome. Watson et al. identified several proteins presumably associated with cell defense and secondary metabolism [10]. Despite the ecological and evolutionary importance of nectar, mechanisms controlling its synthesis and secretion remain largely unknown. Orona-Tamayo et al. conducted proteomic study of extrafloral nectaries of Acacia cornigera [51]. The dominant classes that have been identified belonged to carbohydrate metabolism, and protein synthesis and degradation. The gravitropic response of gynophores plays an essential role in reproductive organ development, the molecular mechanisms of which are largely unexplored. The comparative proteomics of gravity stimulated and natural growth of gynophores revealed an array of differentially regulated proteins putatively involved in cell defense and signal transduction, among others [52]. 2.5 Seed Gallardo et al. sequentially analyzed the seed proteome of barrel medic, which comprised of storage proteins, and those involved in cell division and carbon metabolism [53–55]. The seed storage proteins were found to be the most abundant, www.proteomics-journal.com

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which decreased under low nitrogen conditions. The proteome of germinating seeds revealed 111 Trx-linked proteins, which have marked overlap with the Trx-linked proteins of cereals [56]. Intertissue compartmentalization of proteins has relevance to the nutritional value of legume seeds. The change in seed proteome profile is indicative of a metabolic shift from a highly active to a quiescent state as the embryo assimilates nutrients during seed filling [55]. The first proteome map of pea seed revealed 156 proteins, highlighting processing of storage proteins, particularly 7S globulins. Most nonstorage proteins were found to be associated with cell defense and germination [57]. It is increasingly clear that seed proteins accumulate in protein bodies in the cotyledonary parenchyma cells until they undergo hydrolysis upon germination. Proteins involved in cell division are abundant during early stages of seed development, and their level decreases before the accumulation of major storage proteins during seed filling [53]. Soybean seed proteome displayed 216 proteins that function in metabolism, protein destination and storage, metabolite transport, and cell defense [58, 59]. Agrawal et al. identified 478 seed proteins in five developmental stages of soybean seed [60]. In a comparative proteomic analysis, Gomes et al. reported genotype-dependent protein diversity in soybean seeds and the major groups were storage and lipid metabolism proteins [61]. The seed proteome profile of the EMBRAPA BR-16 appears to be different from the profiles of transgenic soybeans reported earlier [62]. Comprehensive comparison of rice and soybean germinating seed proteomes displayed distinct mechanism for reserves mobilization [63]. Phosphoproteomic analysis of trefoil has provided the molecular explanation of seed proteome and highlighted the abundant proteins, containing ATM-kinase target motifs, X-X-pS/pT-Q-X-X putatively involved in cell proliferation. An overlap of 46.5% proteins was observed between the cotyledons and hypocotyl [64]. The seed proteome of yellow lupin proclaimed 152 nonredundant set of proteins, majority of which belong to defense response [65]. Molecular dissection of soybean seed coat proteomic has revealed the proteins involved in intermediary metabolism, flavonoid biosynthesis, protein folding, and degradation [66]. Proteins involved in translation machineries dominate the initial stages of seed coat differentiation, while stressresponsive proteins dictate the later stages [66]. Furthermore, multiple defense proteins with antifungal activity are abundant in the seed coat as against blanched seed [67].

2.6 Pod Seed storage proteins that serve as a nutrient source for developing seedlings represent pod proteome [10]. Proteomic analysis of trefoil pod revealed 604 proteins that include ribosomal, integral membrane, nucleotide binding, nucleartransport, and LEA proteins [68]. A comprehensive analysis of subterranean and aerial pods of peanut revealed selectively  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

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enhanced expression of photosynthesis and oxidative stress associated proteins during pod swelling [69]. 2.7 Somatic embryos and cell suspension cultures The proteome of cell suspension culture in barrel medic displayed 907 nonredundant proteins involved in TCA, glycolysis, ubiquitin pathway, and secondary metabolism [70]. Similar conclusions were made by a study in cowpea (Vigna unguiculata) [71]. The proteome of cell cultures at the globular stage yielded more than 3000 proteins [72]. Further, proteomic insights into barrel medic somatic embryos, of both the highly embryogenic and its nonembryogenic predecessor lines commenced into 136 proteins with marked differential expression [73]. Additionally, there have been reports of unique proteins in the protoplasts of barrel medic with distinct function in organogenic and embryogenic capabilities of cultured cells [74, 75]. Shoot organogenesis from cotyledonary explants in Vigna radiata highlighted important proteins involved in folding and maturation [76].

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Organelle

While traditional methods to assign proteins to subcellular locations are mostly targeted to a single protein of interest, high-throughput proteomics can associate a large number of proteins with different organelles. Most organellar proteomic studies in legumes have focused on membrane fractions owing to the relevance of cell surface interactions between plant and bacteroid during rhizobial symbiosis (Fig. 3, Supporting Information Fig. 1 and Supporting Information Table 2). 3.1 Apoplast The apoplast proteome includes proteins permanently associated with the ECM and the secreted proteins, also termed the secretome. Most apoplastic studies used suspension cultures [77, 78], leaf apoplasts [79], xylem sap [80], and root cap cells [81]. Soares et al. identified 304 apoplast proteins in leaves of barrel medic comprising PR proteins and those associated with cell wall modification [82]. Additionally, serine proteases and glycoproteins were also identified [83]. Kusumawati et al. examined the secretome of alfalfa and barrel medic and highlighted the significant constituents of the apoplasm [83]. Gupta et al. developed the most comprehensive map of chickpea secretome with identification of 773 proteins [78]. Comparative analysis of chickpea secretome with that of barrel medic, Arabidopsis, and rice revealed that the majority of identified proteins are seemingly species-specific. Liao et al. studied secretome collected from the root exudates of three legume species viz., white lupin, soybean, and cowpea [84]. These proteomes highlighted few species-specific proteins as well as the abundance of signaling proteins secreted into the rhizosphere. Xylem is crucial in transporting water, nutrients and metabolites, and long-distance signaling, modulated by www.proteomics-journal.com

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multivariate proteins as revealed by the proteome of soybean xylem sap [85]. Djordjevic et al. previously investigated the involvement of xylem sap proteins in the autoregulation of nodulation [86]. The phloem sap proteome is quite distinct from that of the xylem sap, which is predominantly represented by proteins involved in signal transduction [87, 88]. The cell wall or ECM proteins account for 10% of its mass [89]. Two independent groups identified 97 [90] and 111 [91] proteins in the ECM of alfalfa. Classical cell wall proteins included wall-modifying proteins and those involved in cell defense and extracellular signaling. Numerous class III secretory peroxidases were implicated in both defense and lignin biosynthesis [90]. The first ECM proteome of crop legume was established by Bhushan et al. in chickpea, which comprised of both structural and functional proteins [92]. The comparison of the cell wall of chickpea with those of barrel medic revealed the recruitment of conserved and unique proteins.

the biogenesis of ribosomal subunits or nucleocytoplasmic trafficking [101]. This study also revealed the presence of chromatin-modifying enzymes and RNA interference proteins. The examination of nuclear phosphoproteome in chickpea unraveled an array of putative phosphoproteins, presumably involved in diverse cellular functions [102].

3.4 Mitochondria The abundant classes of mitochondrial proteins are related to oxidative phosphorylation, pyruvate decarboxylation, citric acid cycle, amino acid degradation, and ATP synthesis, many of which are involved in ROS detoxification [27]. Additionally, many enzymes are organized in the form of “complexosomes” in the mitochondria [103, 104]. The differences in legume mitochondrial complexes might extrapolate to adaptations for elevated energy requirements due to rhizobial symbiosis.

3.2 Microsomal fraction The proteomic analysis of root plasma membrane of barrel medic displayed 78 proteins [93]. Comparison between control and G. intraradices infected roots projected differential regulation of only two proteins viz., H1-ATPase and a predicted glycosyl-phosphatidylinositol-anchored blue copper-binding protein, both potentially located on the periarbuscular membrane. Lefebvre et al. investigated the protein contents of lipid rafts in plasma membranes of barrel medic and elucidated their putative functions [94]. The major membrane proteins in the symbiosome of barrel medic were found to be associated with transport, cytoskeleton modulation, and protein stability [95]. Wienkoop and Saalbach isolated the peribacteroid membrane (PBM) of trefoil and identified 94 proteins including transporters, signaling, and pathogen-responsive proteins [96]. Panter et al. isolated the soybean PBM and identified proteins homologous to HSP70 and HSP60 as well as nodulin 53b and nodulin 26b. The HSPs were hypothesized to be important in symbiosome biogenesis and function [97]. Saalbach et al. studied PBM as well as peribacteroid space (PBS) of pea enabling identification of membrane-specific proteins [98]. In a recent study, Clarke et al. reported 197 proteins in the symbiosome of soybean, putatively involved in cellular processes such as protein folding and degradation, membrane trafficking, and solute transport [99].

3.3 Nucleus Investigation on chickpea nucleus revealed 150 proteins, most of which belonged to signaling and gene regulation followed by proteins involved in DNA replication and transcription [100]. Proteomic analysis of nuclear proteome during seed filling in barrel medic identified 143 proteins, which highlights distinct proteins with possible roles in  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

3.5 Plastid The first plastid proteome in legume was reported from barrel medic, which comprised of 266 proteins [105]. Most of the proteins have been predicted to be involved in nucleic acid-related processes, carbohydrate, and nitrogen/sulfur metabolism together with stress response. Bayer et al. reported 448 proteins in pea chloroplast inclusive of 43 putative novel candidates, highlighting their role in carbohydrate metabolism [106].

3.6 Peroxisomes Peroxisomes, single-membrane-bound organelles are the key in plant responses to abiotic and biotic stresses. Arai et al. succeeded in identifying 92 peroxisomal soybean proteins, including enzymes for fatty acid ␤-oxidation, glyoxylate cycle, photorespiratory glycolate metabolism, and stress response. Interestingly, S-nitrosylation of leaf peroxisome proteins in pea has been shown to have distinct functions in photorespiration, ␤-oxidation, and ROS detoxification [107].

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Stress-responsive proteomes

The advances of stress proteomics, in recent years, have enabled plant biologists to investigate the molecular events associated with stress adaptation. While stress response is a complex biological phenomenon, proteomics investigations could facilitate unique proteome profiles in a spatiotemporal manner. Despite extensive cataloguing of a few thousands of proteins in legumes, functional characterization of the proteomes in a given tissue, developmental phase and environmental cues remains elusive. The following sections www.proteomics-journal.com

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illustrate the progress in stress-responsive proteomics in legumes (Fig. 3, Supporting Information Fig. 1 and Supporting Information Table 3).

4.1 Abiotic stress 4.1.1 Water deficit Over the past decade, extensive proteomic studies have been accomplished to dissect complex molecular mechanism/s of water deficit or dehydration tolerance. Pandey et al. investigated the dehydration-responsive proteome of chickpea and suggested the role of nuclear proteins in dehydration tolerance [108]. Bhushan et al. established that ECM proteins of chickpea are intimately involved in multivariate cellular functions affecting cell wall modification to minimize water loss [109]. Molecular dissection of ECM proteomes of dehydration susceptible and tolerant varieties of chickpea revealed their differing ability to recover from dehydration-induced damage [110]. In a separate study on chickpea, Vessal et al. suggested significant role of HSP and ROS detoxifying enzymes in combating dehydration stress [111]. Furthermore, Subba et al. demonstrated that dehydration stress imposed upon chickpea seedlings affect differential expression of essential proteins, viz., structural proteins, and those involved in ROS detoxification [112]. Dehydration-responsive proteomic studies have also been conducted in grasspea [113], pea [114], and mung bean [115], highlighting similar results. Additionally, proteomic investigations have been attempted to explore the molecular mechanism of dehydration in common bean [116]. Yang et al. demonstrated the role of osmotic stress-responsive proteins on cell-wall porosity and aluminium accumulation in the root tips of common bean [117]. Quantitative proteomic analyses in peanut established the effect of dehydration on three biological processes mainly involved in biomass production, seed germination, and nutritional quality [118]. Serine proteases of lupin were shown to be upregulated in initial phase of water-deficit condition despite the increase in protease inhibitors [119]. The proteomic analyses of soybean seedling under osmotic stress showed higher number of differentially expressed proteins in roots than those in other organs [120]. Region-specific soybean root proteome revealed that the root tips are rich in proteins associated with isoflavonoid pathway as compared to the region away from the tip, which is represented by proteins of lignin synthesis [121]. The impact of dehydration on SNF has been documented in alfalfa [122], barrel medic [123, 124], pea [125], and soybean [126]. Such studies have been conducted using splitroot system approaches [127]. Seedlings of nodulated alfalfa inflicted with dehydration displayed reduced SNF owing to inhibition of nitrogenase activity [122]. The most comprehensive account of nodule proteome so far is that of dehydration inflicted barrel medic inoculated with S. meliloti, which displayed 377 differentially regulated proteins [123]. The findings suggested that the bacteroid proteins involved in SNF  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

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and carbon metabolism are reduced with concomitant suppression of host proteins [123, 124].

4.1.2 Flooding The deleterious effect of flooding or waterlogging on legume proteome has been extensively studied in soybean. The organ-based flooding-responsive proteome of root, leaf, and hypocotyl of developing seedlings displayed downregulation of cytoplasm and chloroplast localized proteins [128]. Effects of flooding stress when assessed on early symbiotic interaction between soybean roots and B. japonicum revealed 219 differentially expressed proteins. The upregulation of proteins, associated with defense, protein synthesis, and metabolism, was found to be positively correlated with increase in RHs during early symbiotic differentiation [129]. Furthermore, flooding-responsive proteins were found to undergo PTMs primarily glycosylation [130], ubiquitination [22], and phosphorylation [131]. Komatsu et al. explored the mechanistic basis of flooding response in presence of abscisic acid (ABA) and indicated the involvement of proteins associated to cell organization, vesicular transport, and glycolysis [132]. It was hypothesized that the involvement of ABA in flooding tolerance might be accomplished through the regulation of zinc finger proteins and transducin. Study on soybean seedlings, subjected to flooding and low oxygen, revealed downregulation of storage and trafficking proteins figuratively implying a mechanistic overlap between the two distinct stress conditions [133]. The impact of flooding in soybean was also estimated on ERenriched fraction [130]. Nanjo et al. established a flooding tolerance index for tolerant, moderately tolerant, and hypersensitive varieties of soybean. Proteomic analysis revealed a synergistic relationship between RNA processing and flooding stress indicator proteins that dictate the flooding tolerance index [134, 135]. The similar set of flooding stress-responsive proteins were found to decrease in the soybean mutants, which exhibited better adaptation [136]. The postflooding recovery mechanisms have also been implicated in flooding tolerance in soybean [137, 138]. High-throughput proteomic studies of soybean seedling during postflooding recovery suggest possible roles of ROS detoxification [137] and cell wall restructuring [138].

4.1.3 Salinity Extensive proteomic studies have been carried out in legumes to unravel the underlying mechanisms of salt tolerance [139]. Proteomic investigation of hypersalinity response of soybean indicated altered expression of proteins of key metabolic functions [140–143]. PR proteins and ROS detoxification enzymes were reported to be downregulated by hypersalinity in pea [144]. A global proteomic analysis of salt stress response of grasspea (Lathyrus sativus) revealed an upregulation of proteins associated with cell defense and signaling, besides protein biogenesis [145]. Yin et al. pointed out that Ca2+ ion www.proteomics-journal.com

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improves the salt stress tolerance by activation of different metabolic pathways [146]. Genotypic variation and ploidy cause major differences in tolerance to salinity stress. Comparative proteomic study of soybean suggests that salt-tolerant genotype survived hypersalinity by improved ROS-detoxification and efficient energy supply machineries [147]. Salt tolerance in relation to ploidy has been demonstrated by Wang et al. with the observation that diploid black locust (Robinia pseudoacacia) is hypersensitive to salt stress when compared with tetraploid plants [148].

4.1.4 Cold Several groups independently investigated cold stress response in legumes through proteomic approaches. Coleman et al. compared six genotypes of alfalfa and demonstrated that charged and/or low molecular weight proteins are induced in cold-hardened plants [149]. Similarly, Gerloff et al. showed that soluble proteins of alfalfa roots are increased during hardening with concomitant increase in antioxidants [150]. The proteins associated with photosynthesis and cell defense are upregulated in response to chilling stress in pea [151] and soybean [152]. Badowiec et al. examined the effects of chilling stress in germinated pea and suggested that such stress influences accumulation of proteins associated with Ca2+ -dependent signal transduction pathways, and those promoting cell division and expansion [153].

4.1.5 Heat Preliminary works with the seedlings of soybean, alfalfa, and barrel medic subjected to heat stress revealed several heat-responsive proteins, presumably involved in energy metabolism and cell defense [154–157]. Ahsan et al. observed heat stress-induced upregulation of HSP70, CPN-60 ␤, and ChsHSP in all tissues of soybean [158]. The role of LEA proteins in heat stress tolerance has been well documented in Australian chestnut (Castanospermum australe) [159].

4.1.6 Dark and UV–B irradiation The molecular responses of legumes to dark conditions are poorly understood. To date, there has been a single report on proteome profile of peanut under darkness, which revealed that the differentially expressed proteins are predominantly involved in energy metabolism, protein folding, and degradation [160]. The effect of solar ultraviolet-B (UV-B) irradiation in soybean proteome highlighted the upregulation of photosynthesis-related proteins [161].

4.1.7 Ozone Soybean productivity is adversely affected by ozone (O3 ) as demonstrated by Ahsan et al. [162]. The findings revealed that several proteins involved in photosystem I/II and carbon assimilation are downregulated, whereas proteins associated with antioxidant defense are upregulated. Further, Galant  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

et al. showed that redox-sensitive proteins are affected in soybean, suggesting the role of ozone flux and increased antioxidants in the suppression of ozone-induced damage [163]. 4.1.8 Mineral deficiency and heavy metal toxicity Iron deficiency has a negative effect on legume production worldwide. The effects of Fe-deficiency on barrel medic grown in soil containing CaCO3 showed enhanced expression of proteins involved in riboflavin biosynthesis [164]. In a similar study, Alves et al. established the role of boron in lupin development via modulation of proteins associated with key metabolic pathways [165]. Under conditions of phosphate deficiency, nodule growth in soybean is significantly affected with concomitant changes in proteome profile [166]. Aluminium (Al) toxicity also reduces legume production on acidic soil. Investigation of Al-toxicity indicated differential expression of an array of functional proteins viz., chaperones, GSTs, chalcone-related synthetase, GTP-binding proteins, ABC transporter, and ATP-binding protein in soybean [167] and alfalfa [168]. Manganese overload has been shown to cause brown depositions in the cowpea leaf with the corresponding increase in peroxidases [79]. Navascues et al. observed the progressive downregulation of key enzymes involved in sucrose metabolism and ROS detoxification in Al-inflicted L. corniculatus [169]. Sobkowiak and Deckert reported cadmium (Cd2+ ) induced altered expression of several proteins in soybean that include histone H2B, chalcone synthase, and glutathione transferase [170]. Cd2+ -toxicity has also been documented in Caesalpinia peltophoroides [171], green gram [172], and barrel medic [173] by comparative proteomic investigation. Green gram, a Cd2+ sensitive legume, when analyzed during a combined treatment of iron and cadmium, portrayed high-abundance of proteins associated with nutrient acquisition [172]. 4.2 Biotic stress Diseases caused by biotrophic pathogens, such as rusts, downy mildews, and powdery mildews, are major limiting factors affecting legume production. Multivariate proteomic studies have been successfully accomplished to understand the molecular mechanisms underlying biotic stress tolerance. Legumes are affected by severe root rot diseases caused by oomycete pathogens, mainly from the genera Phytophthora, Pythium, and Aphanomyces. Among these pathogens, Aphanomyces euteiches is the most destructive in areas with temperate and humid climates. Soybean seedlings when infected with Phytophthora sojae revealed differentially expressed proteins involved in protein synthesis, secondary metabolism, photosynthesis, and photorespiration [174], accompanied by altered composition of xylem sap [175]. Schenkluhn et al. characterized the root proteome of barrel medic under the combined effect of symbionts and pathostress A. euteiches, and constructed pathostressresponsive protein profile [24]. The differential proteome www.proteomics-journal.com

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comprised of proteins involved in symbiosis such as antioxidants, symbiosis-specific signaling, and Ran-binding proteins of nucleocytoplasmic signaling. Additionally, pathostressresponsive proteins were predominantly PR proteins, Kunitztype proteinase inhibitors, lectin, and phytoalexin synthesis [176, 177]. Comparative proteomics of pea infected by powdery mildew revealed several of the potential registrants associated with disease tolerance [178]. Ascochyta blight of legumes is caused by a complex comprised of Ascochyta pisi, A. pinodes (teleomorph Mycosphaerella pinodes), and Phoma medicaginis. The compatible reaction of pea with M. pinodes, revealed 31 disease-responsive proteins presumably involved in metabolism, transcription, and cell defense [179]. Similar observations were made by Borges et al. in common bean inflicted with Pseudocercospora griseola [180]. Proteomic analysis of a compatible interaction between pea and downy mildew pathogen, Peronospora viciae, revealed upregulation of many potential stress-responsive proteins [181]. Several rust species can infect grain and forage legumes, most of which belong to genus Uromyces. The proteomic studies in Uromyces striatus infecting barrel medic were carried out by Castillejo Sanchez et al. [182], whereas Phakopsora pachyrhizi on soybean was conducted by Ganiger et al. [183] and Wang et al. [184]. Late leaf spot, caused by Phaeoisariopsis personata, reduces pod yield and affects the fodder and seed quality in Arachis sp. The disease progression was proteomically analyzed in A. diogoi [185]. The proteomics study in bean infected with rust fungi demonstrated the activation of R-gene-mediated defense during infection [186]. Vascular wilt of chickpea, caused by Fusarium oxysporum f. sp. ciceri (Foc), direct altered expression of metabolismrelated proteins, followed by recruitment of registrants involved in cell defense [187]. The aflatoxin-induced proteins of groundnut are involved in signal transduction, nucleotide synthesis, and defense against disease invasion. Furthermore, the proteins downregulated in response to aflatoxin are involved in carbohydrate metabolism, vesicular trafficking, and transcriptional regulation [188]. Incompatible interaction of Colletotrichum gloeosporioides on mung bean was found to influence the altered expression of disease resistance proteins, including PR-10, chitinase II, and cysteine proteases [189]. MYMIV infects several legumes, and molecular characterization of mung bean proteome challenged with MYMIV demonstrated role of many proteins in disease progression. The proteomic analyses indicated significant role of SA in defense mechanism caused by activation of calmodulin [190, 191]. Insects cause severe damages both through direct feeding, as vectors or by providing infection sites for phytopathogens. The leaf proteome of pea inflicted with aphid, Acyrthosiphon pisum, displayed reduction of photosynthesis and amino acid biosynthesis, besides enhanced accumulation of wound signal molecules such as LOXs and LAPs, and activation of the antioxidants [192].  C 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

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Future perspectives

Legume research has made steady advance since the last decade owing to the increase in the number of completely sequenced genomes, besides availability of ESTs and protein sequences. It is due to the advances in sample preparation, high-resolution protein separation, and sensitive MS/MS techniques. Technical limitations, however, still exist, for example, validation of extraction efficiency and purity, and identification of low-abundant proteins. Unlike yeast and mammalian proteomics, plant proteomics including those of legumes faces intrinsic challenges because the proteomes are less amenable to data analysis due to greater genomic diversity. Furthermore, the processing methodologies are inherently skill-based and are difficult to automate. Reproducibility in protein separation, gel-based methods in particular, remains a challenge. The exploration of complementary technologies, either alone or in combination, assumes more prominent roles in future legume proteomics, whether in proteome expression profiling or screening of protein association networks. The current status of proteomics research assumes new hope for the legume community. The incidences of legume proteomics are no more restricted to generating proteome reference maps, but to understanding key proteins for adaptation under myriad stress environments of biotic and abiotic nature. Nonetheless, the number of proteins is surprisingly low considering the expected number of proteins in a cell, tissue, or organ for any given legume species. Targeted proteomics in legume with careful selection of the species would provide information relevant to a particular biological question. This is particularly important given that the aim is not likely linked with identifying the protein components, but in their potential utilization. Therefore, the future efforts must be endeavored toward bridging the gaps by saturation of genome and proteome maps in legumes, and eventually utilization of these repertoires in legume improvement programs. This work was supported by grants (38(1385/14/EMR-II)) from the Council of Scientific and Industrial Research (CSIR), Govt. of India. We also thank the CSIR for providing predoctoral fellowship to D.R. and S.G., and the Department of Biotechnology (DBT), Govt. of India for post-doctoral fellowship to D.G. We thank Mr. Jasbeer Singh for illustrations and graphical representation in the manuscript. The authors have declared no conflict of interest.

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