CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Functional Plant Biology   
Functional Plant Biology
Journal Banner
  Plant Function & Evolutionary Biology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Research Fronts
Reviews
Evolutionary Reviews
Sample Issue
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow PrometheusWiki
blank image
PrometheusWiki
Protocols in ecological and environmental plant physiology

 

Article << Previous     |     Next >>   Contents Vol 41(7)

Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle

Ana Laura Furlan A B C , Eliana Bianucci A , María del Carmen Tordable A , Stella Castro A and Karl-Josef Dietz B

A Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto. Ruta 36, Km 601, 5800 Río Cuarto, Córdoba, Argentina.
B Biochemistry and Physiology of Plants, Bielefeld University, D-33501 Bielefeld, Germany.
C Corresponding author. Email: afurlan@exa.unrc.edu.ar

Functional Plant Biology 41(7) 704-713 http://dx.doi.org/10.1071/FP13311
Submitted: 24 October 2013  Accepted: 29 January 2014   Published: 26 March 2014


 
PDF (657 KB) $25
 Export Citation
 Print
  
Abstract

Drought stress is one of the most important environmental factors that affect plant growth and limit biomass production. Most studies focus on drought stress development but the reversibility of the effects receives less attention. Therefore, the present work aims to explore the biological nitrogen fixation (BNF) of the symbiotic association between peanut (Arachis hypogaea L.) and Bradyrhizobium sp. during a drought–recovery cycle with a focus on the response of enzyme activity and gene expression of the antioxidant system. Peanuts exposed to drought stress had impaired BNF, as indicated by lower nitrogenase activity, and decreased leghaemoglobin content; the latter was reversed to control values upon rehydration. Previous results demonstrated that reactive oxygen species (O2·- and H2O2) were accumulated as a consequence of drought stress, suggesting that nodules experience oxidative stress. In addition, marker transcripts responsive to drought, abscisic acid and H2O2 were upregulated. Increased transcript levels of glutathione reductase were associated with an increased enzyme activity but superoxide dismutase and glutathione S-transferase activities were unchanged, despite upregulated gene transcription. In contrast, increased activity of ascorbate peroxidase (APX) was unrelated with changes in cytosolic APX transcript levels suggesting isogene specificity. In conclusion, the work exemplarily demonstrates the efficient and dynamic regulation of antioxidant enzymes and marker compounds during drought cycling, which is likely to be a prerequisite for functional optimisation of nodule metabolism.

Additional keywords: antioxidant system, Arachis hypogaea, biological nitrogen fixation, oxidative stress, reactive oxygen species.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
CrossRef | PubMed |

Amako K, Chen GX, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant & Cell Physiology 35, 497–504.

Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods in Enzymology 113, 548–555.
CrossRef | PubMed |

Appleby C, Bergersen F (1980) Preparation and experimental use of leghemoglobin. In ‘Methods for evaluating biological nitrogen fixation’. (Ed FJ Bergersen) pp. 315–335. (John Wiley: Chichester)

Arrese-Igor C, González EM, Gordon AJ, Minchin FR, Gálvez L, Royuela M, Cabrerizo PM, Aparicio-Tejo PM (1999) Sucrose synthase and nodule nitrogen fixation under drought and other environmental stresses. Symbiosis 27, 189–212.

Arrese-Igor C, González EM, Marino D, Ladrera R, Larrainzar E, Gil-Quintana E (2011) Physiological responses of legume nodules to drought. In ‘Plant nutrition and abiotic stress tolerance III. Plant stress 5 (Special issue 1)’. (Eds NA Anjum, F Lopez-Lauri) pp. 24–31. (Global Science Books: Ikenobe, Japan)

Asensio AC, Marino D, James EK, Ariz I, Arrese-Igor C, Aparicio-Tejo PM, Arredondo-Peter R, Moran JF (2011) Expression and localization of a Rhizobium-derived cambialistic superoxide dismutase in pea (Pisum sativum) nodules subjected to oxidative stress. Molecular Plant-Microbe Interactions 24, 1247–1257.
CrossRef | PubMed |

Beauchamp CO, Fridovich I (1973) Isoenzymes of SOD from wheat germ. Biochimica et Biophysica Acta 317, 50–64.
CrossRef | PubMed |

Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytologist 188, 960–976.
CrossRef | PubMed |

Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. The Plant Cell 14, 1391–1403.
CrossRef | PubMed |

Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae 120, 264–270.
CrossRef |

Boote K (1982) Growth stages of peanut (Arachis hypogaea L.). Peanut Science 9, 35–40.
CrossRef |

Bradford M (1976) A rapid sensitive method for the quantification the microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
CrossRef | PubMed |

Bright J, Desikan R, Tancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal 45, 113–122.
CrossRef | PubMed |

Burk R (1996) ‘Soil survey laboratory methods manual, soil survey investigations report 42, version 3.0.’ (National Soil Survey Center: Lincoln, NE, USA).

Collino DJ, Dardanelli JL, Sereno R, Racca RW (2001) Physiological responses of Argentine peanut varieties to water stress. Light interception, radiation use efficiency and partitioning of assimilates. Field Crops Research 70, 177–184.
CrossRef |

Dalton DA (1995) Antioxidant defenses of plants and fungi. In ‘Oxidative stress and antioxidant defenses in biology’. (Ed S Ahmad) pp. 298–355. (Chapman and Hall: New York)

Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proceedings of the National Academy of Sciences of the United States of America 83, 3811–3815.
CrossRef | PubMed |

Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. The Plant Cell 14, S15–S45.

Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. The Journal of Biological Chemistry 280, 12 168–12 180.
CrossRef |

Flohé L, Günzler W (1984) Assays of glutathione peroxidase. Methods in Enzymology 105, 114–120.
CrossRef | PubMed |

Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signalling 11, 861–905.
CrossRef |

Furlan A Llanes A Luna V Castro S 2012 Physiological and biochemical responses to drought stress and subsequent rehydration in the symbiotic association peanut–Bradyrhizobium sp. ISRN Agronomy 2012 Article ID 318083 10.5402/2012/318083

Furlan A, Llanes A, Luna V, Castro S (2013) Abscisic acid mediation in hydrogen peroxide production in peanut under water stress. Biologia Plantarum 57, 555–558.
CrossRef |

Gogorcena Y, Iturbe-Ormaetxe I, Escuredo PR, Becana M (1995) Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiology 108, 753–759.

Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercaptric acid formation. The Journal of Biological Chemistry 249, 7130–7139.

Halliwell B, Gutteridge JMC (1999) ‘Free radicals in biology and medicine.’ 3rd edn. (Oxford University Press, Oxford)

Hardy R, Burns R, Holsten T (1973) Application of the acetylene reduction assay for the measurement of nitrogen fixation. Soil Biology & Biochemistry 5, 47–81.
CrossRef |

Hoagland D, Arnon D (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station Bulletin 347, 1–39.

Hong L, Hu B, Liu X, He CY, Yao Y, Li XL, Li L (2013) Molecular cloning and expression analysis of a new stress-related AREB gene from Arachis hypogaea. Biologia Plantarum 57, 56–62.
CrossRef |

Irigoyen JJ, Emerich DW, Sánchez-Díaz M (1992) Phosphoenolpyruvate carboxylase, malate and alcohol dehydrogenase activities in alfalfa (Medicago sativa) nodules under water stress. Physiologia Plantarum 84, 61–66.
CrossRef |

Jacquot JP, Dietz KJ, Rouhier N, Meux E, Lallement PA, Selles B, Hecker A (2013) Redox regulation in plants: glutathione and “redoxin” related families. In ‘Oxidative stress and redox regulation’. (Eds U Jakob, D Reichmann) pp. 213–231. (Springer Science Business Media: Dordrecht)

Law M, Charles S, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. Biochemical Journal 210, 899–903.

Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiology and Biochemistry 47, 132–138.
CrossRef | PubMed |

Luo M, Liang XQ, Dang P, Holbrook CC, Bausher MG, Lee RD, Guo BZ (2005) Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Plant Science 169, 695–703.
CrossRef |

Marino D, Gonzalez EM, Arrese-Igor C (2006) Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by Paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. Journal of Experimental Botany 57, 665–673.
CrossRef | PubMed |

Marino D, Pucciariello C, Puppo P, Frendo P (2009) The redox state, a referee of the legume–rhizobia symbiotic game. Advances in Botanical Research 52, 115–151.
CrossRef |

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
CrossRef | PubMed |

Morgante CV, Guimarães PM, Martins ACQ, Araújo ACG, Leal-Bertioli SCM, Bertioli DJ, Brasileiro ACM (2011) Reference genes for quantitative reverse transcription-polymerase chain reaction expression studies in wild and cultivated peanut. BMC Research Notes 4, 339
CrossRef | PubMed |

Nakano Y, Asada K (1987) Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant & Cell Physiology 28, 131–140.

Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiology 142, 1364–1379.
CrossRef | PubMed |

Naya L, Ladrera R, Ramos J, Gonzalez EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiology 144, 1104–1114.
CrossRef | PubMed |

Oelze ML, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A, Maurino VG, Dietz KJ (2012) Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals. Journal of Experimental Botany 63, 1297–1313.
CrossRef | PubMed |

op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320–2332.
CrossRef |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
CrossRef | PubMed |

Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. The Plant Journal 31, 319–330.
CrossRef | PubMed |

Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytologist 157, 135–143.
CrossRef |

Puppo A, Rigaud J, Job D (1981) Role of superoxide anion in leghemoglobin autoxidation. Plant Science Letters 22, 353–360.
CrossRef |

Rao MV, Hale BA, Ormrod DP (1995) Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Role of antioxidant enzymes. Plant Physiology 109, 421–432.

Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Annals of Botany 108, 789–795.
CrossRef | PubMed |

Ruijter JM, Ramakers C, Hoogaars W, Bakker O, van den Hoff MJB, Karlen Y, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45
CrossRef | PubMed |

Sassi S, González EM, Aydi S, Arrese-Igor C, Abdely C (2008) 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. Plant and Soil 312, 39–48.
CrossRef |

Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296–302.
CrossRef | PubMed |

Shaedle M, Bassham J (1977) Chloroplast glutathione reductase. Plant Physiology 59, 1011–1012.
CrossRef |

Vincent J (1970) ‘A manual for the practical study of root nodule bacteria, IBP handbook no 15.’ (Blackwell Scientific Publication, Oxford, UK)

Wormuth D, Baier M, Kandlbinder A, Scheibe R, Hartung W, Dietz KJ (2006) Regulation of gene expression by photosynthetic signals triggered through modified CO2 availability. BMC Plant Biology 6, 15
CrossRef | PubMed |

Zabalza A, Gálvez L, Marino D, Royuela M, Arrese-Igor C, González EM (2008) Effects of ascorbate and its immediate precursor, galactono-1,4-lactone on the response of nitrogen-fixing pea nodules to water stress. Journal of Plant Physiology 165, 805–812.
CrossRef | PubMed |

Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytologist 175, 36–50.
CrossRef | PubMed |

Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid induced antioxidant activities in Stylosanthes guianensis. Journal of Experimental Botany 56, 3223–3228.
CrossRef | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2015