Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation

Furlan AL, Bianucci E, Castro S, Dietz K-J (2017)
Plant Science : an International Journal of Experimental Plant Biology 263: 12-22.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Furlan, Ana Laura; Bianucci, Eliana; Castro, Stella; Dietz, Karl-JosefUniBi
Abstract / Bemerkung
Legumes belong to the most important crops worldwide. They increase soil fertility due their ability to establish symbiotic associations with soil microorganisms, known as rhizobia, capable of fixing nitrogen from the atmosphere. However, they are frequently exposed to abiotic stress conditions in particular drought. Such adverse conditions impair the biological nitrogen fixation (BNF) and depend largely on the legume. Therefore, two peanut cultivars with contrasting tolerance to drought, namely the more tolerant EC-98 and the sensitive Granoleico, were investigated to elucidate the relative contribution of BNF to the tolerance to drought. The tolerant cultivar EC-98 sustained growth and BNF similar to the control condition despite the reduced water potential and photosynthesis, suggesting the functioning of distinct metabolic pathways that contributed to enhance the tolerance. The biochemical and metabolomics approaches revealed that nodules from the tolerant cultivar accumulated trehalose, proline and gamma-aminobutyric acid (GABA), metabolites with known function in protecting against drought stress. The amide metabolism was severely affected in nodules from the sensitive cultivar Granoleico as revealed by the low content of asparagine and glutamine in the drought stressed plants. The sensitive cultivar upon rehydration was unable to re-establish a metabolism similar to well-watered plants. This was evidenced by the low level of metabolites and, transcripts and specific activities of enzymes from the carbon (sucrose synthase) and nitrogen (glutamine synthetase) metabolism which decreased below the values of control plants. Therefore, the increased content of metabolites with protective functions under drought stress likely is crucial for the full restoration upon rehydration. Smaller changes of drought stress-related metabolites in nodule are another trait that contributes to the effective control of BNF in the tolerant peanut cultivar (EC-98). Copyright © 2017 Elsevier B.V. All rights reserved.
Plant Science : an International Journal of Experimental Plant Biology
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Furlan AL, Bianucci E, Castro S, Dietz K-J. Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation. Plant Science : an International Journal of Experimental Plant Biology. 2017;263:12-22.
Furlan, A. L., Bianucci, E., Castro, S., & Dietz, K. - J. (2017). Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation. Plant Science : an International Journal of Experimental Plant Biology, 263, 12-22. doi:10.1016/j.plantsci.2017.06.009
Furlan, A. L., Bianucci, E., Castro, S., and Dietz, K. - J. (2017). Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation. Plant Science : an International Journal of Experimental Plant Biology 263, 12-22.
Furlan, A.L., et al., 2017. Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation. Plant Science : an International Journal of Experimental Plant Biology, 263, p 12-22.
A.L. Furlan, et al., “Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation”, Plant Science : an International Journal of Experimental Plant Biology, vol. 263, 2017, pp. 12-22.
Furlan, A.L., Bianucci, E., Castro, S., Dietz, K.-J.: Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation. Plant Science : an International Journal of Experimental Plant Biology. 263, 12-22 (2017).
Furlan, Ana Laura, Bianucci, Eliana, Castro, Stella, and Dietz, Karl-Josef. “Metabolic features involved in drought stress tolerance mechanisms in peanut nodules and their contribution to biological nitrogen fixation”. Plant Science : an International Journal of Experimental Plant Biology 263 (2017): 12-22.

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Daten bereitgestellt von Europe PubMed Central.

Importance of Lupinus albescens in agricultural and food-related areas: A review.
Confortin TC, Todero I, Luft L, Soares JF, Mazutti MA, Zabot GL, Tres MV., 3 Biotech 8(10), 2018
PMID: 30333950

101 References

Daten bereitgestellt von Europe PubMed Central.

Prospects for future climate change and the reasons for early action.
MacCracken MC., J Air Waste Manag Assoc 58(6), 2008
PMID: 18581807
Prospects for future climate change and the reasons for early action.
Edgerton SA, MacCracken MC, Jacobson MZ, Ayala A, Whitman CE, Trexler MC., J Air Waste Manag Assoc 58(11), 2008
PMID: 19044154
Global Synthesis of Drought Effects on Food Legume Production.
Daryanto S, Wang L, Jacinthe PA., PLoS ONE 10(6), 2015
PMID: 26061704

IPCC, 2014
Processes contributing to N2–fixation insensitivity to drought in the soybean cultivar Jackson
Serraj, Crop Sci. 36(), 1996
Nitrogen accumulation and nodule activity of field-grown 'Jackson' soybean in response to water deficits.
Serraj R, Bona S, Purcell LC, Sinclair TR., Field Crops Res. 52(1/2), 1997
PMID: IND20633069
Water-deficit effects on carbon and nitrogen metabolism of pea nodules
González, J. Exp. Bot. 49(), 1998
Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress.
Larrainzar E, Wienkoop S, Weckwerth W, Ladrera R, Arrese-Igor C, Gonzalez EM., Plant Physiol. 144(3), 2007
PMID: 17545507
The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants.
Naya L, Ladrera R, Ramos J, Gonzalez EM, Arrese-Igor C, Minchin FR, Becana M., Plant Physiol. 144(2), 2007
PMID: 17468213
Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery.
Larrainzar E, Wienkoop S, Scherling C, Kempa S, Ladrera R, Arrese-Igor C, Weckwerth W, Gonzalez EM., Mol. Plant Microbe Interact. 22(12), 2009
PMID: 19888822
Physiological responses of N2-fixing legumes to water limitation
González, 2015
The effect of water stress on nitrogen-fixing root nodules. I. Effects on the physiology of detached soybean nodules
Sprent, New Phytol. 70(), 1971
Differential organ-specific response to salt stress and water deficit in nodulated bean (Phaseolus vulgaris)
Verdoy, Plant Cell Environ. 27(), 2004
Effect of water stress on nitrogen fixation and nodule structure of common bean
Ramos, Pesq. Agropec. Bras. 38(), 2003
Stress-Induced Declines in Soybean N2 Fixation Are Related to Nodule Sucrose Synthase Activity.
Gordon AJ, Minchin FR, Skot L, James CL., Plant Physiol. 114(3), 1997
PMID: 12223754
et al., Drought effects on carbon exchange and nitrogen fixation in pigeon pea (Cajanus cajan L.)
Nandwal, J. Plant Physiol. 138(), 1991
Enhanced expression of Rhizobium etli cbb₃ oxidase improves drought tolerance of common bean symbiotic nitrogen fixation.
Talbi C, Sanchez C, Hidalgo-Garcia A, Gonzalez EM, Arrese-Igor C, Girard L, Bedmar EJ, Delgado MJ., J. Exp. Bot. 63(14), 2012
PMID: 22511804
The role of sucrose synthase in the response of soybean nodules to drought
González, J. Exp. Bot. 46(), 1995
Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls.
Nasr Esfahani M, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS., Plant J. 79(6), 2014
PMID: 24947137
Nitrogenase activity: photosynthesis and nodule water potential in soybean plants experiencing water-deprivation
Durand, J. Exp. Bot. 38(), 1987
Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean (Phaseolus vulgaris L.)
Ramos, Ann. Bot. 83(), 1999
Involvement of ureides in nitrogen fixation inhibition in soybean
Serraj R, Vadez V V, Denison RF, Sinclair TR., Plant Physiol. 119(1), 1999
PMID: 9880371
Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean
Vadez, Physiol. Plant. 110(), 2000
Phloem Glutamine and the Regulation of O2 Diffusion in Legume Nodules.
Neo HH, Layzell DB., Plant Physiol. 113(1), 1997
PMID: 12223605
The feedback mechanism of nitrate inhibition of nitrogenase activity in soybean may involve asparagine and/or products of its metabolism
Bacanamwo, Physiol. Plant. 100(), 1997
Is N-feedback involved in the inhibition of nitrogen fixation in drought-stressed Medicago truncatula?
Gil-Quintana E, Larrainzar E, Arrese-Igor C, Gonzalez EM., J. Exp. Bot. 64(1), 2012
PMID: 23175536
Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.
Gil-Quintana E, Larrainzar E, Seminario A, Diaz-Leal JL, Alamillo JM, Pineda M, Arrese-Igor C, Wienkoop S, Gonzalez EM., J. Exp. Bot. 64(8), 2013
PMID: 23580751
A proteomic approach reveals new actors of nodule response to drought in split‐root grown pea plants
Irar S, Gonzalez EM, Arrese‐Igor C, Marino D., Physiol Plant 152(4), 2014
PMID: IND601259736
Drought stress provokes the down-regulation of methionine and ethylene biosynthesis pathways in Medicago truncatula roots and nodules.
Larrainzar E, Molenaar JA, Wienkoop S, Gil-Quintana E, Alibert B, Limami AM, Arrese-Igor C, Gonzalez EM., Plant Cell Environ. 37(9), 2014
PMID: 24471423
The redox state: a referee of the legume-rhizobia symbiotic game
Marino, Adv. Bot. Res.: Oxid. Stress Redox Regul Plants 52(), 2009
Recent insights into antioxidant defenses of legume root nodules.
Becana M, Matamoros MA, Udvardi M, Dalton DA., New Phytol. 188(4), 2010
PMID: 21039567
Inhibition of nitrogen fixation in symbiotic Medicago truncatula upon Cd exposure is a local process involving leghaemoglobin.
Marino D, Damiani I, Gucciardo S, Mijangos I, Pauly N, Puppo A., J. Exp. Bot. 64(18), 2013
PMID: 24151304
Evidence for transcriptional and post-translational regulation of sucrose synthase in pea nodules by the cellular redox state.
Marino D, Hohnjec N, Kuster H, Moran JF, Gonzalez EM, Arrese-Igor C., Mol. Plant Microbe Interact. 21(5), 2008
PMID: 18393622
Sulfenylated proteins in the Medicago truncatula-Sinorhizobium meliloti symbiosis.
Oger E, Marino D, Guigonis JM, Pauly N, Puppo A., J Proteomics 75(13), 2012
PMID: 22634402
Nodulation of groundnut by Bradyrhizobium: a simple infection process by crack entry
Boogerd, FEMS Microbiol. Rev. 21(), 1997

USDA-United, 2016
Condiciones de la sequía regional del ciclo /12 y su influencia en el cultivo de maní
Morla, 2011
Genotypic Variation in Peanut for Transpiration Response to Vapor Pressure Deficit
Devi MJyostna, Sinclair ThomasR, Vadez Vincent., Crop Sci. 50(1), 2010
PMID: IND44318589
Comparison of common bean (Phaseolus vulgaris L.) genotypes for nitrogen fixation tolerance to soil drying
Devi, Plant Soil 364(), 2013
The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems
Peoples, Symbiosis 48(), 2009
Evaluación y selección de germoplasma de maní (Arachis hypogaea L.) tolerante a estrés hídrico
Faustinelli, Ciencia y Tecnología de los cultivos industriales: Maní (), 2012
Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle
Furlan AL, Bianucci E, Tordable MdC, Castro S, Dietz KJ., Funct. Plant Biol. 41(7), 2014
PMID: IND500904030
Scholander PF, Hammel HT, Hemmingsen EA, Bradstreet ED., Proc. Natl. Acad. Sci. U.S.A. 52(1), 1964
PMID: 16591185

Somasegaran, 1994
Methods for evaluating nitrogen fixation by nodulated legumes in the field
Peoples, ACIAR Monograph 11(VII), 1989
Carbon isotope discrimination and photosynthesis
Farquhar, Annu. Rev. Plant Phys. 40(), 1989
N2-fixation in field settings: estimations based on natural 15N abundance
Shearer, Aust. J. Plant. Physiol. 13(), 1986
Photosynthetic and respiratory C costs of N and P nutrition in the dual symbiosis of a mycorrhizal legume
Mortimer, Soil Biol. Biochem. 40(), 2008
Arbuscular mycorrhizae affect the N and C economy of nodulated Phaseolus vulgaris (L.) during NH4+ nutrition
Mortimer PE, Perez-Fernandez MA, Valentine AJ., Soil Biol. Biochem. 41(10), 2009
PMID: IND44272989
MeltDB: a software platform for the analysis and integration of metabolomics experiment data.
Neuweger H, Albaum SP, Dondrup M, Persicke M, Watt T, Niehaus K, Stoye J, Goesmann A., Bioinformatics 24(23), 2008
PMID: 18765459
FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry.
Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O., Anal. Chem. 81(24), 2009
PMID: 19928838
Open source clustering software.
de Hoon MJ, Imoto S, Nolan J, Miyano S., Bioinformatics 20(9), 2004
PMID: 14871861
Java Treeview--extensible visualization of microarray data.
Saldanha AJ., Bioinformatics 20(17), 2004
PMID: 15180930
Regulation of gene expression by photosynthetic signals triggered through modified CO2 availability.
Wormuth D, Baier M, Kandlbinder A, Scheibe R, Hartung W, Dietz KJ., BMC Plant Biol. 6(), 2006
PMID: 16916444
The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress.
Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ., J. Biol. Chem. 280(13), 2005
PMID: 15632145
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data.
Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF., Nucleic Acids Res. 37(6), 2009
PMID: 19237396
Effect of some compounds on glutamine synthetase isoforms activity from Triticale seedling leaves
Bielawski, Acta Physiol. Plant. 16(), 1994
Sucrose synthase of soybean nodules.
Morell M, Copeland L., Plant Physiol. 78(1), 1985
PMID: 16664189
What is principal component analysis?
Ringner M., Nat. Biotechnol. 26(3), 2008
PMID: 18327243
Natural genetic variation in plant photosynthesis.
Flood PJ, Harbinson J, Aarts MG., Trends Plant Sci. 16(6), 2011
PMID: 21435936
Improving yield by exploiting mechanisms underlying natural variation of photosynthesis.
Lawson T, Kramer DM, Raines CA., Curr. Opin. Biotechnol. 23(2), 2012
PMID: 22296828
Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions.
Muscolo A, Junker A, Klukas C, Weigelt-Fischer K, Riewe D, Altmann T., J. Exp. Bot. 66(18), 2015
PMID: 25969553
Transcriptomic Changes Drive Physiological Responses to Progressive Drought Stress and Rehydration in Tomato.
Iovieno P, Punzo P, Guida G, Mistretta C, Van Oosten MJ, Nurcato R, Bostan H, Colantuono C, Costa A, Bagnaresi P, Chiusano ML, Albrizio R, Giorio P, Batelli G, Grillo S., Front Plant Sci 7(), 2016
PMID: 27066027
Plant responses to water deficit.
Bray EA., Trends Plant Sci. 2(2), 1997
PMID: c6696
Jatropha curcas seedlings show a water conservation strategy under drought conditions based on decreasing leaf growth and stomatal conductance
Diaz-Lopez, Agric. Water Manag. 105(), 2012
Bradyrhizobium sp. inoculation ameliorates oxidative protection in cowpea subjected to long-term composted tannery sludge amendment
Moraes, Eur. J. Soil Biol. 76(), 2016
The rules of engagement in the legume-rhizobial symbiosis.
Oldroyd GE, Murray JD, Poole PS, Downie JA., Annu. Rev. Genet. 45(), 2011
PMID: 21838550
Rhizobium-legume symbioses: the crucial role of plant immunity.
Gourion B, Berrabah F, Ratet P, Stacey G., Trends Plant Sci. 20(3), 2014
PMID: 25543258
Tolerance of common bean to long-term osmotic stress is related to nodule carbon flux and antioxidant defenses, evidence from two cultivars with contrasting tolerance
Sassi, Plant Soil 312(), 2008
Trehalose metabolism in plants.
Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M., Plant J. 79(4), 2014
PMID: 24645920
Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions.
El-Bashiti T, Hamamci H, Oktem HA, Yucel M., Plant Sci. 169(1), 2005
PMID: IND43721819
Isolation and characterization of drought-related trehalose 6-phosphate-synthase gene from cultivated cotton (Gossypium hirsutum L.).
Kosmas SA, Argyrokastritis A, Loukas MG, Eliopoulos E, Tsakas S, Kaltsikes PJ., Planta 223(2), 2005
PMID: 16086175
Accumulation of γ-aminobutyric acid in nodulated soybean in response to drought stress
Serraj, Physiol. Plant. 102(), 1998
Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions.
Signorelli S, Dans PD, Coitino EL, Borsani O, Monza J., PLoS ONE 10(3), 2015
PMID: 25775459
Proline: a multifunctional amino acid.
Szabados L, Savoure A., Trends Plant Sci. 15(2), 2009
PMID: 20036181
Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery
Parida, Acta Phys. Plant. 30(), 2008
Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach.
Evers D, Lefevre I, Legay S, Lamoureux D, Hausman JF, Rosales RO, Marca LR, Hoffmann L, Bonierbale M, Schafleitner R., J. Exp. Bot. 61(9), 2010
PMID: 20406784
Concerted changes in N and C primary metabolism in alfalfa (Medicago sativa) under water restriction.
Aranjuelo I, Tcherkez G, Molero G, Gilard F, Avice JC, Nogues S., J. Exp. Bot. 64(4), 2013
PMID: 23440170
Nitrogen fixation control under drought stress. Localized or systemic?
Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, Gonzalez EM., Plant Physiol. 143(4), 2007
PMID: 17416644
TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase.
Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL., Plant Physiol. 144(2), 2007
PMID: 17468221
The molecular biology of glutamine synthetase in higher plants
Forde, 1989
Photorespiratory metabolism and nodule function: behavior of Lotus japonicus mutants deficient in plastid glutamine synthetase.
Garcia-Calderon M, Chiurazzi M, Espuny MR, Marquez AJ., Mol. Plant Microbe Interact. 25(2), 2012
PMID: 22007601
Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen
Parsons, Plant Cell Environ. 16(), 1993
Carbohydrate metabolism in drought- stressed leaves of pigeonpea (Cajanus cajan)
Keller, J. Exp. Bot. 44(), 1993
Nitrate assimilation in Lotus japonicus.
Marquez AJ, Betti M, Garcia-Calderon M, Pal'ove-Balang P, Diaz P, Monza J., J. Exp. Bot. 56(417), 2005
PMID: 15911564


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