Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach

Vilchez JI, Niehaus K, Dowling DN, Gonzalez-Lopez J, Manzanera M (2018)
FRONTIERS IN MICROBIOLOGY 9: 17.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Vilchez, Juan I.; Niehaus, KarstenUniBi; Dowling, David N.; Gonzalez-Lopez, Jesus; Manzanera, Maximino
Abstract / Bemerkung
Drought tolerance of plants such as tomato or pepper can be improved by their inoculation with rhizobacteria such as Microbacterium sp. 3J1. This interaction depends on the production of trehalose by the microorganisms that in turn modulate the phyto-hormone profile of the plant. In this work we describe the characterization of metabolic changes during the interaction of pepper plants with Microbacterium sp. 3J1 and of the microorganism alone over a period of drought. Our main findings include the observation that the plant responds to the presence of the microorganism by changing the C and N metabolism based on its glutamine and alpha-ketoglutarate content, these changes contribute to major changes in the concentration of molecules involved in the balance of the osmotic pressure. These include sugars and amino-acids; the concentration of antioxidant molecules, of metabolites involved in the production of phytohormones like ethylene, and of substrates used for lignin production such as ferulic and sinapic acids. Most of the altered metabolites of the plant when inoculated with Microbacterium sp. 3J1 in response to drought coincided with the profile of altered metabolites in the microorganism alone when subjected to drought, pointing to a response by which the plant relies on the microbe for the production of such metabolites. To our knowledge this is the first comparative study of the microbe colonized-plant and microbe alone metabolomes under drought stress.
Stichworte
PGPR; Microbacterium sp 3J1; Capsicum annum; trehalose; desiccation-tolerance; RDTE; comparative metabolomics
Erscheinungsjahr
2018
Zeitschriftentitel
FRONTIERS IN MICROBIOLOGY
Band
9
Art.-Nr.
17
ISSN
1664-302X
Page URI
https://pub.uni-bielefeld.de/record/2918657

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Vilchez JI, Niehaus K, Dowling DN, Gonzalez-Lopez J, Manzanera M. Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach. FRONTIERS IN MICROBIOLOGY. 2018;9: 17.
Vilchez, J. I., Niehaus, K., Dowling, D. N., Gonzalez-Lopez, J., & Manzanera, M. (2018). Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach. FRONTIERS IN MICROBIOLOGY, 9, 17. doi:10.3389/fmicb.2018.00284
Vilchez, Juan I., Niehaus, Karsten, Dowling, David N., Gonzalez-Lopez, Jesus, and Manzanera, Maximino. 2018. “Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach”. FRONTIERS IN MICROBIOLOGY 9: 17.
Vilchez, J. I., Niehaus, K., Dowling, D. N., Gonzalez-Lopez, J., and Manzanera, M. (2018). Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach. FRONTIERS IN MICROBIOLOGY 9:17.
Vilchez, J.I., et al., 2018. Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach. FRONTIERS IN MICROBIOLOGY, 9: 17.
J.I. Vilchez, et al., “Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach”, FRONTIERS IN MICROBIOLOGY, vol. 9, 2018, : 17.
Vilchez, J.I., Niehaus, K., Dowling, D.N., Gonzalez-Lopez, J., Manzanera, M.: Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach. FRONTIERS IN MICROBIOLOGY. 9, : 17 (2018).
Vilchez, Juan I., Niehaus, Karsten, Dowling, David N., Gonzalez-Lopez, Jesus, and Manzanera, Maximino. “Protection of Pepper Plants from Drought by Microbacterium sp 3J1 by Modulation of the Plant's Glutamine and alpha-ketoglutarate Content: A Comparative Metabolomics Approach”. FRONTIERS IN MICROBIOLOGY 9 (2018): 17.

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Russell DA, Garlena RA, Hatfull GF., Microbiol Resour Announc 8(5), 2019
PMID: 30714032
Effects of Copper and pH on the Growth and Physiology of Desmodesmus sp. AARLG074.
Buayam N, Davey MP, Smith AG, Pumas C., Metabolites 9(5), 2019
PMID: 31052259
Metabolomics in Plant Priming Research: The Way Forward?
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PMID: 29899301

106 References

Daten bereitgestellt von Europe PubMed Central.


Abeles F., Morgan P., Saltveit M.., 1992
Chloroplast-located flavonoids can scavenge singlet oxygen.
Agati G, Matteini P, Goti A, Tattini M., New Phytol. 174(1), 2007
PMID: 17335499
Polyamines: molecules with regulatory functions in plant abiotic stress tolerance.
Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF., Planta 231(6), 2010
PMID: 20221631
Metabolomic and proteomic changes in the xylem sap of maize under drought.
Alvarez S, Marsh EL, Schroeder SG, Schachtman DP., Plant Cell Environ. 31(3), 2007
PMID: 18088330
Physiological, metabolic, and molecular responses of plants to abiotic stress
Arbona V., Manzi M., Zandalinas S., Vives-Peris V., Pérez-Clemente R., Gómez-Cadenas A.., 2017
Structure-activity relationships for antioxidant activities of a series of flavonoids in a liposomal system.
Arora A, Nair MG, Strasburg GM., Free Radic. Biol. Med. 24(9), 1998
PMID: 9641252
Roles of glycine betaine and proline in improving plant abiotic stress resistance
Ashraf M., Foolad M.., 2007
Amino Acid and protein metabolism in bermuda grass during water stress.
Barnett NM, Naylor AW., Plant Physiol. 41(7), 1966
PMID: 16656387
Comprehensive metabolite profiling of Sinorhizobium meliloti using gas chromatography-mass spectrometry.
Barsch A, Patschkowski T, Niehaus K., Funct. Integr. Genomics 4(4), 2004
PMID: 15372312
Lignin biosynthesis.
Boerjan W, Ralph J, Baucher M., Annu Rev Plant Biol 54(), 2003
PMID: 14503002
Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level.
Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P, Bacic A, Roessner U., Mol Plant 5(2), 2011
PMID: 22207720
Responses of the pea (Pisum sativum L.) leaf metabolome to drought stress assessed by nuclear magnetic resonance spectroscopy
Charlton A., Donarski J., Harrison M., Jones S., Godward J., Oehlschlager S.., 2008
Understanding plant responses to drought — from genes to the whole plant
Chaves MM, Maroco JP, Pereira JS., Funct. Plant Biol. 30(3), 2003
PMID: IND44640437
Analysis of Drought-Induced Proteomic and Metabolomic Changes in Barley (Hordeum vulgare L.) Leaves and Roots Unravels Some Aspects of Biochemical Mechanisms Involved in Drought Tolerance.
Chmielewska K, Rodziewicz P, Swarcewicz B, Sawikowska A, Krajewski P, Marczak L, Ciesiolka D, Kuczynska A, Mikolajczak K, Ogrodowicz P, Krystkowiak K, Surma M, Adamski T, Bednarek P, Stobiecki M., Front Plant Sci 7(), 2016
PMID: 27512399
Assessment of SCAR markers to design real-time PCR primers for rhizosphere quantification of Azospirillum brasilense phytostimulatory inoculants of maize.
Couillerot O, Poirier MA, Prigent-Combaret C, Mavingui P, Caballero-Mellado J, Moenne-Loccoz Y., J. Appl. Microbiol. 109(2), 2010
PMID: 20141548
Plant drought stress: effects, mechanisms and management
Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S.., 2009
Metabolite profiling for plant functional genomics.
Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, Willmitzer L., Nat. Biotechnol. 18(11), 2000
PMID: 11062433
Metabolic relationships of putrescine, GABA and alkaloids in cell and root cultures of Solanaceae
Flores H., Filner P.., 1985
Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis.
Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C., Plant J. 30(1), 2002
PMID: 11967092
The phenylpropanoid pathway in Arabidopsis.
Fraser CM, Chapple C., Arabidopsis Book 9(), 2011
PMID: 22303276
Alleviation of Drought Stress and Metabolic Changes in Timothy (Phleum pratense L.) Colonized with Bacillus subtilis B26.
Gagne-Bourque F, Bertrand A, Claessens A, Aliferis KA, Jabaji S., Front Plant Sci 7(), 2016
PMID: 27200057
Identifying the ligated amino acid of archaeal tRNAs based on positions outside the anticodon.
Galili T, Gingold H, Shaul S, Benjamini Y., RNA 22(10), 2016
PMID: 27516383
A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms.
Garcia-Fontana C, Narvaez-Reinaldo JJ, Castillo F, Gonzalez-Lopez J, Luque I, Manzanera M., Front Microbiol 7(), 2016
PMID: 28066383
A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria
Glick BR, Penrose DM, Li J., J. Theor. Biol. 190(1), 1998
PMID: 9473391
Promotion of plant growth by bacterial ACC deaminase
Glick B., Todorovic B., Czarny J., Cheng Z., Duan J., Mcconkey B.., 2007
Properties of bacterial endophytes and their proposed role in plant growth.
Hardoim PR, van Overbeek LS, Elsas JD., Trends Microbiol. 16(10), 2008
PMID: 18789693
Metabolite analyses of grain from maize hybrids grown in the United States under drought and watered conditions during the 2002 field season.
Harrigan GG, Stork LG, Riordan SG, Ridley WP, Macisaac S, Halls SC, Orth R, Rau D, Smith RG, Wen L, Brown WE, Riley R, Sun D, Modiano S, Pester T, Lund A, Nelson D., J. Agric. Food Chem. 55(15), 2007
PMID: 17608427
Implication of phenolic compounds and amino acids in tolerance against net blotch disease in barley (Hordeum vulgare L.)
Hendawey M., Gharib M., Marei T., Mohammed A.., 2014
An increase in the content of cell wall-bound phenolics correlates with the productivity of triticale under soil drought.
Hura T, Hura K, Dziurka K, Ostrowska A, Baczek-Kwinta R, Grzesiak M., J. Plant Physiol. 169(17), 2012
PMID: 22980393
Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses.
Jakab G, Ton J, Flors V, Zimmerli L, Metraux JP, Mauch-Mani B., Plant Physiol. 139(1), 2005
PMID: 16113213
Xeroprotectants for the stabilization of biomaterials.
Julca I, Alaminos M, Gonzalez-Lopez J, Manzanera M., Biotechnol. Adv. 30(6), 2012
PMID: 22814234
Exploring the temperature-stress metabolome of Arabidopsis.
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL., Plant Physiol. 136(4), 2004
PMID: 15557093
Gamma aminobutyric acid (GABA) and plant responses to stress
Kinnersley A., Turano F.., 2000
GMD@CSB.DB: the Golm Metabolome Database.
Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D., Bioinformatics 21(8), 2004
PMID: 15613389
Sensitivity of the WRF model to advection and diffusion schemes for simulation of heavy rainfall along the baiu front
Kusaka H., Crook A., Knievel J., Dudhia J.., 2005
Polyamines: essential factors for growth and survival.
Kusano T, Berberich T, Tateda C, Takahashi Y., Planta 228(3), 2008
PMID: 18594857
Advances in polyamine research in 2007.
Kusano T, Yamaguchi K, Berberich T, Takahashi Y., J. Plant Res. 120(3), 2007
PMID: 17351711
Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins.
Lambertsen L, Sternberg C, Molin S., Environ. Microbiol. 6(7), 2004
PMID: 15186351
Nitrogen use efficiency. 2. Amino acid metabolism
Lea PJ, Azevedo RA., Ann. Appl. Biol. 151(3), 2007
PMID: IND43981821
Ferulic acid pretreatment enhances dehydration-stress tolerance of cucumber seedlings
Li D.-M., Nie Y.-X., Zhang J., Yin J.-S., Li Q., Wang X.-J.., 2013
Analysis of copy number variations among diverse cattle breeds.
Liu GE, Hou Y, Zhu B, Cardone MF, Jiang L, Cellamare A, Mitra A, Alexander LJ, Coutinho LL, Dell'Aquila ME, Gasbarre LC, Lacalandra G, Li RW, Matukumalli LK, Nonneman D, Regitano LC, Smith TP, Song J, Sonstegard TS, Van Tassell CP, Ventura M, Eichler EE, McDaneld TG, Keele JW., Genome Res. 20(5), 2010
PMID: 20212021
Trehalose metabolism in plants.
Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M., Plant J. 79(4), 2014
PMID: 24645920
Cold, salinity and drought stresses: an overview.
Mahajan S, Tuteja N., Arch. Biochem. Biophys. 444(2), 2005
PMID: 16309626
Glutamate, Ornithine, Arginine, Proline, and Polyamine Metabolic Interactions: The Pathway Is Regulated at the Post-Transcriptional Level.
Majumdar R, Barchi B, Turlapati SA, Gagne M, Minocha R, Long S, Minocha SC., Front Plant Sci 7(), 2016
PMID: 26909083
High survival and stability rates of Escherichia coli dried in hydroxyectoine.
Manzanera M, Vilchez S, Tunnacliffe A., FEMS Microbiol. Lett. 233(2), 2004
PMID: 15063506
Metabolism and function of polyamines in plants: recent development (new approaches)
Martin-Tanguy J.., 2001
Plant growth-promoting bacteria confer resistance in tomato plants to salt stress.
Mayak S, Tirosh T, Glick BR., Plant Physiol. Biochem. 42(6), 2004
PMID: 15246071
Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter.
Medrano H, Escalona JM, Bota J, Gulias J, Flexas J., Ann. Bot. 89 Spec No(), 2002
PMID: 12102515
Polyamines and abiotic stress in plants: a complex relationship.
Minocha R, Majumdar R, Minocha SC., Front Plant Sci 5(), 2014
PMID: 24847338
Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco.
Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA., Plant Cell 20(6), 2008
PMID: 18577660
Homogenization of linear elastic properties of short-fiber reinforced composites – A comparison of mean field and voxel-based methods
Müller V., Kabel M., Andrä H., Böhlke T.., 2015
Tall fescue endophyte effects on tolerance to water-deficit stress.
Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL., BMC Plant Biol. 13(), 2013
PMID: 24015904
Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids.
Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K, Michael AJ, Tohge T, Yamazaki M, Saito K., Plant J. 77(3), 2013
PMID: 24274116
Rapid method for isolation of desiccation-tolerant strains and xeroprotectants.
Narvaez-Reinaldo JJ, Barba I, Gonzalez-Lopez J, Tunnacliffe A, Manzanera M., Appl. Environ. Microbiol. 76(15), 2010
PMID: 20562279

AUTHOR UNKNOWN, 2005
Salt-tolerant rootstock increases yield of pepper under salinity through maintenance of photosynthetic performance and sinks strength.
Penella C, Landi M, Guidi L, Nebauer SG, Pellegrini E, San Bautista A, Remorini D, Nali C, Lopez-Galarza S, Calatayud A., J. Plant Physiol. 193(), 2016
PMID: 26918569
NO is involved in spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes.
Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y, He X, Zhang X, Ma X, Huang L, Yan Y., Protoplasma 253(5), 2015
PMID: 26338203
Drought-related secondary metabolites of barley (Hordeum vulgare L.) leaves and their metabolomic quantitative trait loci.
Piasecka A, Sawikowska A, Kuczynska A, Ogrodowicz P, Mikolajczak K, Krystkowiak K, Gudys K, Guzy-Wrobelska J, Krajewski P, Kachlicki P., Plant J. 89(5), 2017
PMID: 27880018
Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants
Piquemal J., Lapierre C., Myton K., O'connell A., Schuch W., Grima-Pettenati J.., 1998
Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1.
Quecine MC, Araujo WL, Rossetto PB, Ferreira A, Tsui S, Lacava PT, Mondin M, Azevedo JL, Pizzirani-Kleiner AA., Appl. Environ. Microbiol. 78(21), 2012
PMID: 22865062
Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids
Ralph J., Lundquist K., Brunow G., Lu F., Kim H., Schatz P.., 2004
Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants.
Rodriguez-Salazar J, Suarez R, Caballero-Mellado J, Iturriaga G., FEMS Microbiol. Lett. 296(1), 2009
PMID: 19459961
Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry.
Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L., Plant J. 23(1), 2000
PMID: 10929108
Zinc Excess Triggered Polyamines Accumulation in Lettuce Root Metabolome, As Compared to Osmotic Stress under High Salinity.
Rouphael Y, Colla G, Bernardo L, Kane D, Trevisan M, Lucini L., Front Plant Sci 7(), 2016
PMID: 27375675
Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45
Sandhya V, SK. Z. Ali, Grover Minakshi, Reddy Gopal, Venkateswarlu B., Biol. Fertil. Soils 46(1), 2009
PMID: IND44283030
Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.
Sauter M, Moffatt B, Saechao MC, Hell R, Wirtz M., Biochem. J. 451(2), 2013
PMID: 23535167
Hypothesis/review: Contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress
Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ., Plant Sci. 193-(), 2012
PMID: IND44785223
Compartmentation of GABA metabolism raises intriguing questions.
Shelp BJ, Mullen RT, Waller JC., Trends Plant Sci. 17(2), 2012
PMID: 22226724
Rhizobitoxine modulates plant-microbe interactions by ethylene inhibition.
Sugawara M, Okazaki S, Nukui N, Ezura H, Mitsui H, Minamisawa K., Biotechnol. Adv. 24(4), 2006
PMID: 16516430
Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants.
Thalmann M, Pazmino D, Seung D, Horrer D, Nigro A, Meier T, Kolling K, Pfeifhofer HW, Zeeman SC, Santelia D., Plant Cell 28(8), 2016
PMID: 27436713
The roles of polyamines during the lifespan of plants: from development to stress.
Tiburcio AF, Altabella T, Bitrian M, Alcazar R., Planta 240(1), 2014
PMID: 24659098
Bacterial seed endophytes: genera, vertical transmission and interaction with plants
Truyens S., Weyens N., Cuypers A., Vangronsveld J.., 2015
The cinnamate/monolignol pathway
Umezawa T.., 2010
Centering, scaling, and transformations: improving the biological information content of metabolomics data.
van den Berg RA, Hoefsloot HC, Westerhuis JA, Smilde AK, van der Werf MJ., BMC Genomics 7(), 2006
PMID: 16762068
Plant Drought Tolerance Enhancement by Trehalose Production of Desiccation-Tolerant Microorganisms.
Vilchez JI, Garcia-Fontana C, Roman-Naranjo D, Gonzalez-Lopez J, Manzanera M., Front Microbiol 7(), 2016
PMID: 27746776
Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria.
Vurukonda SS, Vardharajula S, Shrivastava M, SkZ A., Microbiol. Res. 184(), 2015
PMID: 26856449
Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1.
Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK., Proc. Natl. Acad. Sci. U.S.A. 112(2), 2014
PMID: 25550508
Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress.
Witt S, Galicia L, Lisec J, Cairns J, Tiessen A, Araus JL, Palacios-Rojas N, Fernie AR., Mol Plant 5(2), 2011
PMID: 22180467
Ethylene biosynthesis and its regulation in higher plants
Yang S., Hoffman N.., 1984
Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops.
Yang S, Vanderbeld B, Wan J, Huang Y., Mol Plant 3(3), 2010
PMID: 20507936
Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance.
Yobi A, Wone BW, Xu W, Alexander DC, Guo L, Ryals JA, Oliver MJ, Cushman JC., Mol Plant 6(2), 2012
PMID: 23239830
β-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress.
Zanella M, Borghi GL, Pirone C, Thalmann M, Pazmino D, Costa A, Santelia D, Trost P, Sparla F., J. Exp. Bot. 67(6), 2016
PMID: 26792489
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