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Physiological and biochemical changes in different sugar beet genotypes infected with root-knot nematode

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Abstract

Ten genotypes of sugar beet plant either monogerm or multigerm seeds were screened under greenhouse conditions for both susceptibility and biochemical reaction to root-knot nematode (RKN) Meloidogyne incognita. All the tested genotypes were susceptible to nematode infection according to the number of root galls and gall indices. All infected genotypes exhibited significant reduction in chlorophyll a, b and carotenoids compared to non-infected ones. The total indole acetic acid and total phenolic compounds contents (mean of both shoot and root) increased significantly in most infected genotypes compared to non-infected genotypes except Disk-01-99 and Monte Rosa as well as LP16 and LP15 genotypes, respectively. Also, total polyamine contents (putrescine, spermidine and spermine) showed significant increases in response to infection with nematodes in all genotypes. The same trend was observed in lipid peroxidation expressed with malondialdehyde content in all tested genotypes. Activities of polyphenol oxidase, peroxidase, superoxide dismutase and catalase enzymes were also induced in most infected genotypes compared with non-infected genotypes. Generally, infection with RKNs induced the appearance of new protein bands at molecular masses 303, 288, 42 and 37 KDa in all infected genotypes. The differentiation in the appearance and/or disappearance of protein bands according to susceptibility to infection reflects the variation between genotypes in defense against infection.

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Abbreviations

CAT:

Catalase

H2O2 :

Hydrogen peroxide

IAA:

Indole acetic acid

MDA:

Malondialdehyde

OD:

Optical density

PAL:

Phenyl alanine ammonia lyase

PDAB:

Para-dimethylamino-benzoic acid

PA:

Polyamine

POX:

Peroxidase

PPO:

Polyphenol oxidase

Put:

Putrescine

RKNs:

Root-knot nematodes

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Spd:

Spermidine

Spm:

Spermine

TBA:

Thiobarbituric acid

TCA:

Trichloro acetic acid

References

  • Abd El-Monem AA (2007) Polyamines as modulator of wheat growth, metabolism and productivity under high temperature stress. PhD thesis, Faculty of Science, Ain Shams University, Cairo, Egypt

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  PubMed  CAS  Google Scholar 

  • Ayesh AM, Rowayshed GH, Deabes MM (2002) Inhibitory effect of some food additives on biogenic amines formation in beef sausages trials. Egypt J Nut 17:197–202

    Google Scholar 

  • Berger S, Benediktyova Z, Matous K, Benfig K, Mueller MJ, Medbal L, Roitsch T (2007) Visualization of dynamics of plant–pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58:797–806

    Article  PubMed  CAS  Google Scholar 

  • Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332

    Article  PubMed  CAS  Google Scholar 

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530

    Article  CAS  Google Scholar 

  • Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW (1999) Lipochitin oligosaccharides from Rhizobium leguminosarum bv. Viciae reduce auxin transport capacity in Vicia sativa subsp nigra roots. Mol Plant Microbe Interact 12:839–844

    Article  CAS  Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inzé D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732

    PubMed  CAS  Google Scholar 

  • Cavalcanti FR, Resende ML, Lima SP, Silveira JA, Oliveira JT (2007) Activities of antioxidant enzymes and photosynthetic responses in tomato pre-treated by plant activators and inoculated by Xanthomonas vesicatoria. Physiol Mol Plant Pathol 68:198–208

    Article  Google Scholar 

  • Chaerle L, Leinonen I, Jones HG, Straeten DVD (2007) Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. J Exp Bot 58:773–784

    Article  PubMed  CAS  Google Scholar 

  • Chen JX, Wang XF (2006) Plant physiology experimental guide. Higher Education Press, Beijing, pp 24–25, 55–56

  • Chen S, Olbrich A, Heyser RL, Eberhard Fritz E, Polle A (2009) Quantitative X-ray microanalysis of hydrogen peroxide within plant cells. Microsc Res Tech 72:49–60

    Article  PubMed  Google Scholar 

  • Danil AD, George CM (1972) Peach seed dormancy in relation to endogenous inhibitors and applied growth substances. J Am Soc Hortic Sci 17:621–624

    Google Scholar 

  • Dewar AM, Cooke DA (2006) Pests. In: Draycott P (ed) Sugar beet. Blackwell Publishing Ltd, Oxford, pp 316–358

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794

    Google Scholar 

  • El-Khallal SM (2007) Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (Jasmonic acid & Salicylic acid): 2-Changes in the antioxidant enzymes, phenolic compounds and pathogen related-proteins. Aust J Basic Appl Sci 1:717–732

    CAS  Google Scholar 

  • Gómez Ros LV, Paradiso A, Gabaldón C, Pedreño MA, de Gara L, Ros Barceló A (2006) Two distinct cell sources of H2O2 in the lignifying Zinnia elegans cell culture system. Protoplasma 227:175–183

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266

    Article  PubMed  Google Scholar 

  • Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway [comment]. Proc Natl Acad Sci 97:2405–2407

    Article  PubMed  CAS  Google Scholar 

  • Huang G, Gao B, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the oesophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 16:376–381

    Article  PubMed  CAS  Google Scholar 

  • Jung S (2004) Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subjected to drought. Plant Sci 166:459–466

    Article  CAS  Google Scholar 

  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux P (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    PubMed  CAS  Google Scholar 

  • Khattab H (2007) The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Aust J Basic Appl Sci 1:56–62

    CAS  Google Scholar 

  • Kong FX, Hu W, Chao SY, Sang WL, Wang LS (1999) Physiological responses of mexicana to oxidative stress of SO2. Environ Exp Bot 42:201–209

    Article  CAS  Google Scholar 

  • Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Indian J Exp Bot 20:412–416

    CAS  Google Scholar 

  • Larsen P, Harbo A, Klungron S, Ashein TA (1962) On the biosynthesis of some indole compounds in Acetobacter xylinum. Physiol Plant 15:552–565

    Article  CAS  Google Scholar 

  • Leng P, Su S, Wei F, Yu F, Duan Y (2009) Correlation between browning, total phenolic content, polyphenol oxidase and several antioxidation enzymes during pistachio tissue culture. Acta Hortic (ISHS) 829:127–132

    CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Wrolstad RE, Acree TE, An H, Decker EA, Penner MH, Reid DS, Schwartz SJ, Shoemaker CF, Sporns P (eds) Current protocols in food analytical chemistry (CPFA). John Wiley and Sons, New York, pp F4.3.1–F4.3.8

  • Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J Exp Bot 52:419–426

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes—the rhizobium–legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant Soil 255:105–119

    Article  CAS  Google Scholar 

  • Mathesius U (2008) Auxin—at the root of nodule development? Funct Plant Biol 35:651–668

    Article  CAS  Google Scholar 

  • Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    Article  PubMed  CAS  Google Scholar 

  • Melo GA, Shimizu MM, Mazzafera P (2006) Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry 67:277–285

    Article  PubMed  CAS  Google Scholar 

  • Mietz JL, Karmas E (1977) Chemical quality index of canned tuna as determined by high-pressure liquid chromatography. J Food Sci 42:155–158

    Article  CAS  Google Scholar 

  • Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    Article  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • MSTAT-C (1988) MSTAT-C, a microcomputer program for the design, arrangement and analysis of agronomic research. Michigan State University, East Lansing

  • Panella L, Lewellen RT (2007) Broadening the genetic base of sugar beet: introgression from wild relatives. Euphytica 154:383–400

    Article  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  PubMed  CAS  Google Scholar 

  • Polidoros AN, Mylona PV, Scandalios JP (2001) Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant–pathogen interactions and resistance to oxidative stress. Transgenic Res 10:555–569

    Article  PubMed  CAS  Google Scholar 

  • Predieri S, Norma MA, Krizek DT (1995) Influence of UV-B radiation on membrane lipid composition and ethylene of evolution in ‘Doyenne d’Hiver’ pear shoots grown in vitro under different photosynthetic photo fluxes. Environ Exp Bot 35:152–260

    Article  Google Scholar 

  • Rani CI, Veeraragavathatham D, Sanjutha S (2008) Analysis on biochemical basis of root-knot nematode (Meloidogyne incognita) resistance in tomato (Lycopersicon esculentum Mill.) Res. J Agric Biol Sci 4:866–870

    Google Scholar 

  • Reuveni R, Shimoni M, Karchi Z, Kuc J (1992) Peroxidase activity as a biochemical marker for resistance of muskmelon on (Cucumis meb) to Pseudoperonospora cubensis. Phytopathology 82:749–753

    Article  CAS  Google Scholar 

  • Rhee HJ, Kim EJ, Lee JK (2007) Physiological polyamines: simple primordial stress molecules. J Cell Mol Med 11:685–703

    Article  PubMed  CAS  Google Scholar 

  • Rivero RM, Ruiz JM, Garcia PC, Lopez – Lefebre LR, Sanchy E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and water melon plants. Plant Sci 160:315–321

    Article  PubMed  CAS  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    Article  PubMed  CAS  Google Scholar 

  • Sasser JN, Carter C, Hartman KM (1984) Standardization of host suitability studies and reporting of resistance to root-knot nematodes. A Cooperative Publication of the Department of Plant Pathology North Carolina State University and U.S. Agency for International Development. Raleigh, North Carolina, USA, p 7

  • Sheri LH, Ncolas ES, Michae TK, Joanna BG (2000) Comparison of protein expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatograph tandem mass spectrometry. Microbiology 146:2495–2508

    Google Scholar 

  • Soliva RC, Elez P, Sebastián M, Martín O (2001) Evaluation of browning effect on avocado purée preserved by combined methods. Innov Food Sci Emerg Technol 1:261–268

    Article  Google Scholar 

  • Spoel HS, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, DG Jonathan DG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogen. Plant Physiol 141:373–378

    Google Scholar 

  • Van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131

    Article  PubMed  Google Scholar 

  • Velazhahan R, Muthukrishnan S (2004) Transgenic tobacco plants constitutively overexpressing a rice thaumotin-like protein (PR-5) show enhanced resistance to Alternaria alternata. Biol Plant 47:347–354

    Article  Google Scholar 

  • Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Quisenberry SS, Ni X, Tolmay V (2004) Enzymatic chlorophyll degradation in wheat near-isogenic lines elicited by cereal aphid (Homoptera: Aphididae) feeding. J Econ Entomol 97:661–667

    Article  PubMed  CAS  Google Scholar 

  • Wang XH, Replogle A, Davis EL, Mitchum MG (2007) The tobacco cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Mol Plant Pathol 8:423–436

    Article  PubMed  CAS  Google Scholar 

  • Wasson AP, Ramsay K, Jones MG, Mathesius U (2009) Differing requirements for flavonoids during the formation of lateral roots, nodules and root-knot nematode galls in Medicago truncatula. New Phytol 183:167–179

    Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, van Montagu M, Inzé D, van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J J16:4806–4816

    Article  Google Scholar 

  • Zhang S, Klessig DF (2000) In: Hirt H (ed) MAP kinases in plant signal transduction. Springer, Heidelberg, pp 65–84

  • Zhou YH, Yu JQ, Mao WH, Huang LF, Song XS, Nogués S (2006) Genotypic variation on Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants. Plant Cell Physiol 47:192–199

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded by The National Research Centre through the project entitled “The development of integrated management to improve productivity (quantity and quality) of sugar beet”. Project No. 8040716 during 2007–2010.

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Correspondence to Amany A. Abd El-Monem.

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Communicated by B. Barna.

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Korayem, A.M., El-Bassiouny, H.M.S., Abd El-Monem, A.A. et al. Physiological and biochemical changes in different sugar beet genotypes infected with root-knot nematode. Acta Physiol Plant 34, 1847–1861 (2012). https://doi.org/10.1007/s11738-012-0983-1

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  • DOI: https://doi.org/10.1007/s11738-012-0983-1

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