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Medicago Truncatula and Glycine Max: Different Drought Tolerance

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Medicago Truncatula and Glycine Max: Different Drought Tolerance This is an open access article published under a Creative Commons Attribution (CC-BY) License, which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. Article pubs.acs.org/jpr Medicago truncatula and Glycine max:Different Drought Tolerance and Similar Local Response of the Root Nodule Proteome † ‡ ‡ ‡ Erena Gil-Quintana, David Lyon, Christiana Staudinger, Stefanie Wienkoop,*, † and Esther M. Gonzaleź*, † Department of Environmental Sciences, Public University of Navarra, E-31006 Pamplona, Spain ‡ Department of Molecular Systems Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria *S Supporting Information ABSTRACT: Legume crops present important agronomical and environmental advantages mainly due to their capacity to reduce atmospheric N2 to ammonium via symbiotic nitrogen fixation (SNF). This process is very sensitive to abiotic stresses such as drought, but the mechanism underlying this response is not fully understood. The goal of the current work is to compare the drought response of two legumes with high economic impact and research importance, Medicago truncatula and Glycine max, by characterizing their root nodule proteomes. Our results show that, although M. truncatula exhibits lower water potential values under drought conditions compared to G. max, SNF declined analogously in the two legumes. Both of their nodule proteomes are very similar, and comparable down-regulation responses in the diverse protein functional groups were identified (mainly proteins related to the metabolism of carbon, nitrogen, and sulfur). We suggest lipoxygenases and protein turnover as newly recognized players in SNF regulation. Partial drought conditions applied to a split-root system resulted in the local down-regulation of the entire proteome of drought-stressed nodules in both legumes. The high degree of similarity between both legume proteomes suggests that the vast amount of research conducted on M. truncatula could be applied to economically important legume crops, such as soybean. KEYWORDS: Medicago truncatula, soybean, nodule proteome, drought, split-root system ■ INTRODUCTION Legumes have the ability to carry out symbiotic nitrogen fixation (SNF) with nitrogen-fixing soil bacteria known as Grain and forage legumes are grown on around 15% of the fi Earth’s arable surface.1 The grain legume Glycine max rhizobia. Legumes can be classi ed into amide or ureide exporters according to the compounds used for transporting (soybean) is an important source of protein for humans and fi animals, as well as vegetable oil.1 Soybean’seconomic the xed N. In general, amide-exporting legumes, such as M. importance and the large number of researchers who work truncatula, contain indeterminate-type nodules and originated on it have contributed to the development of molecular, in temperate regions. They transport amides, mainly in the genetic, and genomic tools for the species.2 Similarly, in recent form of asparagine and glutamine. Ureide-exporting legumes, decades, Medicago truncatula, a forage legume, has emerged as a such as soybeans, are mostly tropical legumes with determinate- useful model for molecular studies.3,4 The availability of the type nodules and transport mainly allantoin and allantoic acid. complete genome sequences of M. truncatula5 and the soybean Despite the agronomical and environmental advantages of 6 legume crops, their production is limited by environmental plant has facilitated the genomic and proteomic studies of 11 these two species. Having the genome available is key for constraints, drought being one of the most harmful stresses. protein identification by mass spectrometry and, consequently, The regulation of SNF under drought conditions involves for proteomic research. Diverse proteome studies of different various factors, mainly internal oxygen availability, N-feedback fi plant organs, cell cultures, and organelles have been conducted regulation, and carbon limitation. Despite research in the eld, on M. truncatula and G. max under different abiotic stress the molecular-level interactions between the cited factors and conditions (for a review, see refs 7 and 8, respectively). The the SNF regulation mechanism(s) are not fully understood. plant fraction of M. truncatula nodules subjected to drought has Recently, the local regulation of SNF in diverse legumes, been characterized, with a nodule proteome database for this including M. truncatula and soybean plants, has been 10,12,13 species being established.9 Additionally, a brief study on demonstrated under drought stress. These studies soybean nodule proteins under drought stress has also been documented.10 Apart from this, the drought response of legume Received: July 4, 2015 plants has hardly been investigated at the proteome level. © XXXX American Chemical Society A DOI: 10.1021/acs.jproteome.5b00617 J. Proteome Res. XXXX, XXX, XXX−XXX Journal of Proteome Research Article dismiss the generally accepted role of amides and ureides as (w/v) PVP, and 1 mM PMSF). The homogenates were being the molecules involved in inhibiting SNF under drought centrifuged at 20000g at 4 °C for 30 min. Supernatants were conditions. However, it remains unclear whether there are local collected, and soluble proteins were precipitated overnight at changes in the nodule proteome, as in the SNF process, or −20 °C after adding 5 volumes of precooled acetone. Pellets whether systemic signals are involved. Moreover, it has been recovered by centrifugation at 10000g at 4 °C for 10 min were reported that SNF is a more drought-sensitive process in air-dried and resuspended in 300 μL of solubilization buffer (8 ff − ureide-exporting nodules, such as those of soybean plants, than M urea bu er, 100 mM NH4HCO3,pH8 8.5, 5 mM DTT). in the amide exporters such as Medicago.14 Nevertheless, The samples were diluted (1:4) in buffer (25 mM − reports concerning the possibly distinct responses to drought NH4HCO3,pH88.5, 10% (v/v) acetonitrile and 5 mM μ stress of ureide- versus amide-exporting legumes are rare. CaCl2) and aliquots containing 100 g of protein were digested In the present study, the drought response of the nodule overnightat37°C under rotation using Poroszyme- proteome of two model legumes, M. truncatula and G. max,is immobilized trypsin beads (1:20, v/v, Applied Biosystems, compared, leading to the identification of shared stress Life Technologies). After centrifugation for bead removal, the responses as well as unique proteome features of the two obtained peptide mixtures were desalted using SPEC C18 legumes. By using a split-root system (SRS), whereby watered columns according to the manufacturer’s instructions (Varian, and drought-treated nodules shared the same aerial part, one Agilent Technologies). Finally, the desalted digest solutions can observe the local effect of drought stress in the legume were dried, and the pellets were stored at −80 °C until use. nodule proteome resulting in a greater understanding of the Prior to the mass spectrometric measurement, the protein molecular mechanisms regulating SNF. Additionally, this is the digest pellets were dissolved in 0.1% (v/v) formic acid. The first study demonstrating that comparative proteomics across protein digests (5 μg) were analyzed via shotgun nano-LC-ultra related species can improve the functional proteome character- (Eksigent system, Axel Semrau GmbH) using a monolithic ization. The work demonstrates a strategy for determining how reversed-phase column (Chromolith 150 × 0.1 mm; Merck, molecular data may be transferable between legume species, Darmstadt) directly coupled to an LTQ-Orbitrap XL mass such as from model legumes to crop legume species, which is spectrometer (Thermo Scientific, Rockford, IL) operated with an important step forward for the legume research community. Xcalibur (2.0.7 SP1) as described elsewhere.17 The peptides were eluted with a 100 min gradient from 5% to 60% ■ MATERIALS AND METHODS acetonitrile. An Orbitrap-FT analyzer was used for precursor MS1, and an LTQ-XL was used for MS2 mass analyses, Plant Growth Conditions, Split-Root System, and respectively. CID was performed at a normalized collision Drought-Stress Treatment energy of 35. Dynamic exclusion settings were as described in Nodulated M. truncatula Gaertn. cv. Jemalong A17 and G. max ref 18. The mass window for precursor selection was set to 10 (L.) Merr. plants were grown under controlled environmental ppm with a resolution of 30 000 in a mass range from 400 to − − conditions (14 h photoperiod; 400 (μmol m 2 s 1) light 1,800 m/z. intensity; 22 °C and 16 °C day and night temperature; 60 to After the performance of the mass spectrometric analyses, 70% relative humidity) for 12 and 6 weeks, respectively, in the raw files were searched against a composite protein FASTA double pots (600 mL each) to produce SRS. The seedlings file using the Sequest algorithm. The composite protein FASTA fi were inoculated with N2- xing strains: Ensifer meliloti 2011 for file was created by fusing the following databases. For M. M. truncatula; and Bradyrhizobium japonicum strain UPM752 truncatula: (1) Uniprot UniRef100 Medicago; origin: www. for soybean plants, watered with N-free nutrient solutions.15,16 uniprot.org. The search was performed on May 7, 2013; 54 246 The plants were randomly separated into three sets: controls entries. (2) IMGA; origin: http://medicago.org/,64123 (C) received a daily supply of nutrient solution to field capacity entries. (3) DCFI; origin: http://compbio.dfci.harvard.edu/; in both sides of the SRS, whereas drought (D) was achieved by 59 601 entries. For G. max: (1) Uniprot UniRef100 G. max; withholding water and nutrients. In partial drought plants origin: www.uniprot.org. The search was performed on May 15, (PD), one half of the root system was kept at field capacity 2013; 70 318 entries. (2) Gmax_189_protein_annotated.fasta; (PDC), while the other half was kept unwatered (PDD) for 7 from phytozome/v9.0/Gmax/assembly/JGI assembly with days. After this period, four types of nodule samples (C, PDC, 73 320 entries. (3) DCFI; origin: http://compbio.dfci.harvard. PDD, and D) were harvested, immediately frozen in liquid N, edu/.
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