Proteome Analysis of Differentially Displayed Proteins As a Tool for the Investigation of Symbiosis

Natera, Siria; Guerreiro, Nelson; Djordjevic, Michael A.

doi:10.1094/mpmi.2000.13.9.995

Cited by 176 publications

(133 citation statements)

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“…Their data identified 16 root hair proteins whose abundance increased within 12 h of inoculation by Bradyrhizobium japonicum. The accumulation of 11 proteins appeared to require the lipo-chitin Nod signal as they did not respond to inoculation with a B. japonicum nodC mutant, which is defective in Nod signal production.Several recent studies focused proteomics methods on examining the changes in host and symbiont protein profiles during nodule development in L. japonicus, M. truncatula, and Melilotus alba [66][67][68][69][70][71]. Using nano-scale liquid chromatography, Wienkoop and Saalbach [66] analyzed proteins that are affiliated with the symbiosome membrane, which surrounds rhizobia in L. japonicus nodule cells, and identified nutrient-associated transporters, signaling proteins and proteins that are implicated in symbiosome biogenesis.…”

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confidence: 99%

Genetics and functional genomics of legume nodulation

Stacey

Libault

Brechenmacher

et al. 2006

Current Opinion in Plant Biology

252

138

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Gram-negative soil bacteria (rhizobia) within the Rhizobiaceae phylogenetic family (a-proteobacteria) have the unique ability to infect and establish a nitrogen-fixing symbiosis on the roots of leguminous plants. This symbiosis is of agronomic importance, reducing the need for nitrogen fertilizer for agriculturally important plants (e.g. soybean and alfalfa). The establishment of the symbiosis involves a complex interplay between host and symbiont, resulting in the formation of a novel organ, the nodule, which the bacteria colonize as intracellular symbionts. This review focuses on the most recent discoveries relating to how this symbiosis is established. Two general developments have contributed to the recent explosion of research progress in this area: first, the adoption of two genetic model legumes, Medicago truncatula and Lotus japonicus, and second, the application of modern methods in functional genomics (e.g. transcriptomic, proteomic and metabolomic analyses). IntroductionNodulation is a highly host-specific interaction in which, with few exceptions, specific rhizobial strains infect a limited range of plant hosts. Plants secrete (iso)flavonoids that are recognized by the compatible bacteria, resulting in the induction of nodulation genes. These nodulation genes encode enzymes that synthesize a specific lipochitin nodulation signal (Nod signal), which activates many of the early events in the root hair infection process [1][2][3][4][5]. During the infection process, the bacteria enter the plant via the root epidermis and induce the reprogramming of root cortical cell development and the formation of a nodule. In the most well-studied cases, infection occurs through root hairs. The first observable event in the infection process is the curling of the root hair, which likely occurs through the gradual and constant reorientation of the direction of root hair growth. The bacteria become enclosed within the root hair curl where the plant cell wall is degraded, the cell membrane is invaginated and an intracellular tubular structure (i.e. the infection thread) is initiated. It is within this infection thread that the bacteria enter the root hair cell and eventually ramify into the root cortex. Before the infection thread reaches the base of the root hair cell, the root cortical cells are induced to de-differentiate, activating their cell cycle and causing them to divide to form the nodule primordium. In addition to the cortical cells, pericycle cells are also activated and undergo some cell divisions. When the infection thread reaches the cells of the developing primordium, the bacteria are released into cells via endocytosis. Inside a plant cell, the bacteria are enclosed in vacuole-like structures (symbiosomes) in which they differentiate into bacteroids. It is within these symbiosomes that the bacteria convert N 2 to NH 3 . The nodule is a true organ in which there is cellular specialization. For example, in addition to infected plant cells, uninfected plant cells also carry out the function of nitrogen as...

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confidence: 99%

Genetics and functional genomics of legume nodulation

Stacey

Libault

Brechenmacher

et al. 2006

Current Opinion in Plant Biology

252

138

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“…Similar tools were used to identify symbiosis-related proteins in M. truncatula (BestelCorre et al, 2002). Two special studies (Natera et al, 2000;Morris and Djordjevic, 2001) were devoted to the analysis of changes in protein expression in bacteroids compared with free bacteria, and in nodules compared with uninfected roots. Numerous changes were observed representing mostly abundant proteins of known function (like malate dehydrogenase [MDH], DNAK, GroEL, and leghemoglobin).…”

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Proteome Analysis. Novel Proteins Identified at the Peribacteroid Membrane from Lotus japonicus Root Nodules

2003

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The peribacteroid membrane (PBM) forms the structural and functional interface between the legume plant and the rhizobia. The model legume Lotus japonicus was chosen to study the proteins present at the PBM by proteome analysis. PBM was purified from root nodules by an aqueous polymer two-phase system. Extracted proteins were subjected to a global trypsin digest. The peptides were separated by nanoscale liquid chromatography and analyzed by tandem mass spectrometry. Searching the nonredundant protein database and the green plant expressed sequence tag database using the tandem mass spectrometry data identified approximately 94 proteins, a number far exceeding the number of proteins reported for the PBM hitherto. In particular, a number of membrane proteins like transporters for sugars and sulfate; endomembraneassociated proteins such as GTP-binding proteins and vesicle receptors; and proteins involved in signaling, for example, receptor kinases, calmodulin, 14-3-3 proteins, and pathogen response-related proteins, including a so-called HIR protein, were detected. Several ATPases and aquaporins were present, indicating a more complex situation than previously thought. In addition, the unexpected presence of a number of proteins known to be located in other compartments was observed. Two characteristic protein complexes obtained from native gel electrophoresis of total PBM proteins were also analyzed. Together, the results identified specific proteins at the PBM involved in important physiological processes and localized proteins known from nodule-specific expressed sequence tag databases to the PBM.The model legume Lotus japonicus forms nitrogenfixing root nodules after infection by Mesorhizobium loti. The bacteria enter the plant cell by endocytosis, leading to the formation of a new compartment in the plant cell, the symbiosome. This compartment harbors the bacteroids and is surrounded by a peribacteroid membrane (PBM) formed from the plant plasma membrane (PM) during endocytosis of the bacteria (for review, see Verma and Hong, 1996;Whitehead and Day, 1997). The PBM develops further by receiving material from the endomembrane system (see Robertson et al., 1978;Verma and Hong, 1996) and finally forms the structural and functional interface between the symbionts (Robertson et al., 1978). The PBM plays a central role in the exchange of compounds between the organisms (see Udvardi and Day, 1997). To fulfill this role, the PBM is supplied with the specific components, like transporters and enzymes, necessary for the symbiotic exchange processes (see Verma and Hong, 1996;Whitehead and Day, 1997). Several of these activities have been characterized by biochemical and biophysical studies. For example, the activity of P-type H ϩ -ATPase (PATPase) pumping protons from the cytoplasm to the peribacteroid space has been characterized (see Blumwald et al., 1985, and refs. therein). Dicarboxylates are supplied from the plant to the bacteroids, and a specific transporter present in the PBM has been characterized (see Udvardi an...

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“…Analytical gels were visualized by silver staining and protein spots were analyzed using ImageMaster 2D Elite version 3.01 (Amersham Pharmacia Biotech, Uppsala, Sweden). Preparative gels were stained with 0.1% Coomassie brilliant blue R-250 (CBB) and spots were subjected to mass spectrometric (MS) analysis and N-terminal amino acid sequencing 9) .…”

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Characterization of Bacteroid Proteins in Soybean Nodules Formed with Bradyrhizobium japonicum USDA110

2004

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Two-dimensional gel electrophoresis was used to identify differentially displayed proteins of Bradyrhizobium japonicum USDA110 in the symbiotic and non-symbiotic state. When proteome maps were compared and the characterization of bacteroid-specific proteins was performed by N-terminal amino acid sequencing and matrixassisted desorption/ionization time-of-flight mass spectrometry peptide mass fingerprint analysis, putative identity was assigned to 61 bacteroid protein spots, including many metabolic proteins and ABC transporters as well as nitrogenase proteins like NifH. This study shows that proteome analysis will be a useful tool for surveying genes contributing to rhizobial functions in symbiosis.Key words: 2-D gel electrophoresis, Bradyrhizobium japonicum USDA110, MALDI-TOF mass spectrometry, nodule bacteroid, symbiosisSoil bacteria, rhizobia, can form a symbiotic tissue (nodule) in the root of leguminous plants and differentiate to fix nitrogen using photosynthate as an energy source. Since this reaction to produce ammonia from nitrogen gas in the air is useful for agriculture, various researchers have attempted to introduce this system into other crop plants, and genome projects including proteomics have been applied to this complex system to elucidate the molecular mechanism inducing this organogenesis. The proteomic analysis of cultured cells and bacteroids in Sinorhizobium meliloti has provided insight into how microsymbionts alter metabolism to establish an endo-symbiotic relationship with the host plant cells 10) . In soybean, the genomic DNA of Bradyrhizobium japonicum USDA110 has been completely sequenced by the Kazusa DNA Research Institute 5) , and a large scale macroarray analysis is being conducted by comparing gene expression profiles among rhizosphere cells, cultured cells and bacteroids (Minamisawa et al., personal communication). In cooperation with these transcriptome analyses, we compared protein profiles between bacteroids and cultured cells of B. japonicum USDA110 and examined the physiological role of bacteroid specific proteins.Soybean (Glycine max L. Merr. cv. Akishirome) seeds were inoculated with Bradyrhizobium japonicum USDA110 and germinated on moist vermiculite. The seedlings (7-10 days old) were grown hydroponically in a nitrogen-free nutrient solution 17) . Nodules were harvested from plants 4 to 5 weeks after inoculation when the acetylene reduction activity per gram fresh weight of nodules reached a maximum 17) .Bacteroids were isolated from nodules as reported by Day et al. 3) , and were monitored with marker enzyme assays; cytochrome c oxidase for mitochondria 16) , alcohol dehydrogenase for cytosol 15) and b-hydroxybutyrate dehydrogenase (b-HBDH) for bacteroids 14) . High-level b-HBDH

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Proteome Analysis of Differentially Displayed Proteins As a Tool for the Investigation of Symbiosis

Cited by 176 publications

References 60 publications

Genetics and functional genomics of legume nodulation

Genetics and functional genomics of legume nodulation

Proteome Analysis. Novel Proteins Identified at the Peribacteroid Membrane from Lotus japonicus Root Nodules

Characterization of Bacteroid Proteins in Soybean Nodules Formed with Bradyrhizobium japonicum USDA110

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