Journal of Applied & Environmental Microbiology
ISSN (Print): 2373-6747 ISSN (Online): 2373-6712 Website: http://www.sciepub.com/journal/jaem Editor-in-chief: Sankar Narayan Sinha
Open Access
Journal Browser
Go
Journal of Applied & Environmental Microbiology. 2016, 4(5), 93-104
DOI: 10.12691/jaem-4-5-2
Open AccessArticle

Analysis of the Cultivable Endophytic Bacterial Diversity in the Date Palm (Phoenix dactylifera L.) and Evaluation of Its Antagonistic Potential against Pathogenic Fusarium Species that Cause Date Palm Bayound Disease

Rayda Siala1, Ines Ben Chobba1, Tatiana Vallaeys2, Mohamed Ali Triki3, Mouna Jrad3, Manel Cheffi3, Imen Ayedi4, Amine Elleuch1, Ahmad Nemsi5, Frederique Cerqueira6, Radhouane Gdoura7, Noureddine Drira1 and Néji Gharsallah1

1Laboratoire de Biotechnologies Végétales Appliquées à l’Amélioration des Cultures LBVAAC, Faculté des Sciences de Sfax, B.P. 1171, 3000 Sfax, Tunisia

2UMR5119, CC093 Université de Montpellier 2, sciences et techniques, 34095 Montpellier, France.

3Laboratoire d’Amélioration et Protection des Ressources Génétique de l’Olivier, Institut de l’Olivier, BP1078 Université de Sfax, Tunisia

4Laboratoire de microorganismes et de Biomolécules, Equipe Procédés de Criblages moléculaires et cellulaires, Centre de Biotechnologie de Sfax, B.P. 1177, 3018 Sfax, Tunisia

5Laboratoire de Phytopathologie Oasienne, Centre Régional de Recherches en Agriculture Oasienne à Degache, Degache 2260, Tunisia

6Plateforme séquençage-génotypage SFR "Montpellier Environnement Biodiversité", ISEM, Université de Montpellier 2, 34095, Montpellier, France

7Unité de Recherche Toxicologie-Microbiologie Environnementale et Santé (UR11ES70), Faculté des Sciences de Sfax, B.P. 1171, Tunisia

Pub. Date: September 12, 2016

Cite this paper:
Rayda Siala, Ines Ben Chobba, Tatiana Vallaeys, Mohamed Ali Triki, Mouna Jrad, Manel Cheffi, Imen Ayedi, Amine Elleuch, Ahmad Nemsi, Frederique Cerqueira, Radhouane Gdoura, Noureddine Drira and Néji Gharsallah. Analysis of the Cultivable Endophytic Bacterial Diversity in the Date Palm (Phoenix dactylifera L.) and Evaluation of Its Antagonistic Potential against Pathogenic Fusarium Species that Cause Date Palm Bayound Disease. Journal of Applied & Environmental Microbiology. 2016; 4(5):93-104. doi: 10.12691/jaem-4-5-2

Abstract

Biological control still remains an unexploited issue in southern countries such as Tunisia. Thus, the present study focused on the diversity of cultivable endophytic bacteria in the internal tissues (roots and leaves) of Tunisian date palm trees (Phoenix dactylifera L.). In order to assess their antagonistic potential towards date palm pathogens, particularly Fusarium. Indeed, the Genus Fusarium includes the causative agent of the Bayound disease, Fusarium oxysporum, a major treat for date production North Africa. Twenty two bacterial isolates presenting distinct colony morphology on TSA media were selected. The latter were characterized using Gram staining, biochemical tests, and molecular identification techniques based on 16S rRNA gene sequencing. Cultivable endophytic isolates were assigned into seven distinct groups. The species Arthrobacter agilis and Bacillus subtilis exhibited lasting antagonistic properties against a range of Fusarium species including the causing agent of the Bayoud disease, thus demonstrating their strong potential for future applications in the inoculation of date palm trees for biocontrol purposes. The isolates showed extracellular enzymatic activity including cellulase (76, 92%), protease (69, 23%) and amylase (38, 46%). This study thus demonstrates for the first time that the diversity of endophytic bacteria is abundant in date palm trees (Phoenix dactylifera L.) and could present varying biotechnological applications and particularly disease control.

Keywords:
palm date tree endophytic bacteria molecular identification biocontrol Fusarium spp. bayound deseases

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

References:

[1]  Drira N, Benbadis A. 1985. Vegetative Multiplication of Date-Palm (Phoenix dactylifera L.) by Reversion of In Vitro Cultured Female Flower Buds. J Plant Physiol 119: 227-235.
 
[2]  Triki MA, Zouba A, Khoualdia O, Ben Mahamoud O, Takrouni ML, Garnier M, Bové JM, Montarone M, Poupet A, Flores R, Darós JA, Fadda ZGN, Moreno P, Duran-Vila N. 2003. Maladie des feuilles cassantes or brittle leaf disease of date palms in Tunisia: biotic or abiotic disease? J Plant Pathol 85:71-79.
 
[3]  Fernandez M, Lourd M, Ouinten M, Tantaoui A, Geiger JP. 1995. Le Bayoud du palmier dattier, une maladie qui menace la phoéniciculture. Phytoma 469:36-39.
 
[4]  Fernandez D, Ouinten M, Tantaoui A, Geiger JP. 1997. MoIecuIar records of micro-evolution within the Algerian population of Fusarium oxysporum f. sp. albedinis during its spread to new oases. Eur J Plant Pathol 103:485-490.
 
[5]  Hatimi A. 1989. Etude de la réceptivité des sols de deux palmeraies marocaines au Bayoud, p 58. Thèse de troisième cycle, Université Cadi Ayyad, Marrakech.
 
[6]  Maslouhy A. 1989. Contribution à l’étude in vitro et in situ des antagonistes de Fusarium oxysporum f.sp. albedinis, agent causal du Bayoud, p 98. Thèse de troisième cycle, Université Cadi Ayyad, Marrakech.
 
[7]  El Hassni M, J’aiti F, Dihazi A, Ait Barka E, Daayf F, El Hadrami I. 2004. Enhancement of defense responses against Bayoud disease by treatment of date palm seedlings with a hypoaggressive Fusarium oxysporum isolate. J Phyto 152:182-189.
 
[8]  Djerbi M. 1990. Méthodes de diagnostic du Bayoud du palmier dattier. Bull OEPP/EPPO 20:607-613.
 
[9]  Louvet J. 1991. Que devons-nous faire pour lutter contre le Bayoud? p 337-346. Physiologie des arbres et Arbustes en zones arides et semi arides: Groupes d’Etudes d’Arbre, Paris-France.
 
[10]  Haider N, Nabulsi I. 2012. Molecular characterization of Syrian date palm cultivars using plasmid- like DNA markers. Genetika 48:270-4.
 
[11]  Alabouvette C, Lemanceau P, Steinberg C. 1993. Recent advances in the biological control of fusarium wilts. Pest Science 37: 365-373.
 
[12]  M’Piga P, Bélanger RR, Paulitz TC, Benhamou N. 1997. Increased resistance to Fusarium oxysporum f.sp. radicis-lycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain. Physiol Mol Plant Pathol 50: 301-320.
 
[13]  Larkin RP, Fravel DR. 1998. Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Pl Dis 82:1022-1028.
 
[14]  Duijff BJ, Recorbet G, Bakker PAHM, Loper JE, Lemanceau P. 1999. Microbial antagonism at the root level is involved in the suppression of Fusarium wilt by the combination of nonpathogenic Fusarium oxysporum F047 and Pseudomonas putidia WCS358. Phytopathology 89:1073-1079.
 
[15]  Steinberg C, Edel V, Gautheron N, Abadie C, Vallaeys T, Alabouvette C. 1997. Phenotypic characterization of natural populations of Fusarium oxysporum in relation to genotypic characterization. FEMS Microbiol Ecol 24:73-85.
 
[16]  Steinberg C, Edel V, Gautheron N, Vallaeys T, Alabouvette C. 1997. Characterization of Fusarium oxysporum populations by growth parameters evaluation in microtiter plates, p 535-538. In diagnosis and identification of plant pathogens (eds) Dehne HW, Adam G, iekmann M, Frahm J, Mauler-machnik A, Kluwer academic Publisher. Dordrecht.
 
[17]  Chen C, Bauske E, Mussan G, Rodriguez-Kabana R, Kloepper JW. 1995. Biological control of Fusarium wilts on cotton by use of entophytic bacteria. Biol Control 5:83-91.
 
[18]  Benhamou N, Nicole M. 1999. Cell biology of plant immunization against microbial infection: the potential of induced resistance in controlling plant diseases. Plant Physiol Biochem 37: 703-719.
 
[19]  El Hassni M, El Hadrami A, Daayf F, Chérif M, Barka EA, El Hadrami I. 2007. Biological control of bayoud disease in date palm: Selection of microorganisms inhibiting the causal agent and inducing defense reactions. Environ Exp Bot 59:224-234.
 
[20]  Leary JV, Nelson N, Tisserat B, Allingham EA. 1986. Isolation of Pathogenic Bacillus circulans from Callus Cultures and Healthy Offshoots of Date Palm (Phoenix dactylifera L.). Appl Environ Microbiol 52:1173-1176.
 
[21]  Leary JV, Chun WWC. 1989. Pathogenicity of Bacillus circulans to seedlings of date palm (Phoenix dactylifera). Pl Dis 73:353-354.
 
[22]  Thomashow SL. 1996. Biological control of plant root pathogens. Curr Opin Biotechnolo 7:343-347.
 
[23]  Carroll GC, Fokkema NJ and van den Heuvel J. 1986. The Biology of Endophytism in Plants with Particular Reference to Woody Perennials, In: Microbiology of Phyllosphere (eds.), p 205-222. Cambridge University Press, London.
 
[24]  Petrini O. 1991. Fungal Endophyte of Tree Leaves, p 179-197. In microbial ecology of leaves, Andrews J, Hirano SS (eds.). Spring-Verlag, New York.
 
[25]  Jacobs MJ, Bugbee WM, Gabrielson DA. 1985. Enumeration, location and characterization of endophytic bacteria within sugar-beet roots. Can J Bot 63:1262-1265.
 
[26]  Patriquin DG, Dobereiner J. 1978. Light microscopy observations of tetrazolium-reducing bacteria in the endorhizosphere of maize and other grasses in Brazil. Can J Microbiol 24:734-742.
 
[27]  Bell C.R, Dickie GA, Harvey WLG, Chan JWYF. 1995. Endophytic bacteria in grapevine. Can J Microbiol 4:46-53.
 
[28]  Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW. 1997. Bacterial endophytes in agricultural crops. Can J Microbiol 43: 895-914.
 
[29]  Sturz AV, Christie BR, Nowak J. 2000. Bacterial endophytes: Potential role in developing sustainable systems of crop production. Crc Cr Rev Plant Sci 19:1-30.
 
[30]  Rosenblueth M, Martínez-Romero E. 2006. Bacterial endophytes and their interactions with hosts, M P M I 19:827-837.
 
[31]  Germida JJ, Siciliano SD, Freitas JR, Seib AM. 1998. Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43-50.
 
[32]  Kobayashi DY, Palumbo JD. 2000. Bacterial endophytes and their effects on plants and uses in agriculture, p 199–233. In Bacon CW, White JF (eds.), Microbial endophytes. Marcel Dekker, Inc. New York, N.Y.
 
[33]  Gagne S, Richard C, Roussean H, Antoun H. 1987. Xylem-residing bacteria in alfalfa roots. Can J Microbiol 33:996-1000.
 
[34]  Agarwal S, Shende ST. 1987. Tetrazolium reducing microorganisms inside the root of Brassica species. Curr Sci 56: 187-188.
 
[35]  Roos IMM, Hattingh MJ. 1983. Scanning electron microscopy of Pseudomonas syringae pv. morsprunorum on sweet cherry leaves. Phytopathology 108:18-25.
 
[36]  Leben C, Daft GC, Schmitthenner AF. 1968. Bacterial blight of soybeans: population levels of Pseudomonas glycinea in relation to symptom development. Phytopathology 58:1143-1146.
 
[37]  Feng Y, Shen D, Song W. 2006. Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938-945.
 
[38]  Jones P. 1988. Report to the Government of Tunisia on a visit to Centre de Recherche Phoenicicoles. Tozeur, Tunisia, 14th-21st.
 
[39]  Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA. 2000. Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267-274.
 
[40]  Schulz B, Wanke U, Draeger S, Aust HJ. 1993. Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycological Research 97:1447-1450.
 
[41]  Collins CH, Lyne PM. 1984. Microbiological Methods (5th ed.) Butterworths Co, p 65-113. (Publishers), Ltd., London.
 
[42]  Erdogan O, Benlioglu K. 2010. Biological control of Verticillium wilts on cotton by the use of fluorescent Pseudomonas spp. under field conditions. Biol Control 5:39-45.
 
[43]  Korsten L, De Jager ES. 1995. Mode of action of Bacillus subtilis for control of avocado postharvest pathogens. South African Avocado Growers Association Yearbook 18:124-130.
 
[44]  Gerhardt GG, Murray RGF, Wood WA, Krieg NR. 1994. Methods for general and molecular bacteriology, p 13-25. American society for microbiology.
 
[45]  Brosius J, Palmer ML, Kennedy PJ, Noller HF. 1978. Complete nucleotide sequence of 16S ribosomal RNA gene from Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, Biochemistry 75: 4801-4805.
 
[46]  Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences of the United States of America, Evolution 82:6955-6959.
 
[47]  Bottger EC. 1989. Rapid determination of bacterial ribosomal RNA sequences by direct sequencing of enzymatically amplified DNA. FEMS Microbiol Lett 65:171-176.
 
[48]  Thompson JD, Higgins DG, Gibson TJ, Clustal W. 1994. improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
 
[49]  Felsenstein J. 1989. PHYLIP- phylogeny inference package, version. 3. 2. Cladistics 5:164-166.
 
[50]  Saitou N, Nei M. 1987. The Neighbor-Joining method-a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
 
[51]  Crisanto VB, Lourdes IMR, José LB, Josué AH, Idolina FC, Eduardo VC. 2011. A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 339:329-340.
 
[52]  Sapak Z. 2006. Bacterial Endophytes from Oil Palm (Elaeis Guineensis) and Their Antagonistic Activity against Ganoderma Boninense, p 3-6. Master’s thesis. University Putra Malaysia.
 
[53]  Ryan RP, Ryan DJ, Sun YC, Li FM, Wang Y, Dowling DN. 2007. An acquired efflux system is responsible for copper resistance in Xanthomonas strain IG-8 isolated from China. FEMS Microbiol Lett 268:40-46.
 
[54]  Misaghi IJ, Donndelinger CR. 1990. Endophytic bacteria in symptom-free cotton plants. Phytopathology 80:808-811.
 
[55]  Elvira-Recuenco M, Van Vuurde JW. 2000. Natural incidence of endophytic bacteria in pea cultivars under field conditions. Can J Microbiol 46:1036-1041.
 
[56]  Araujo WL, Maccheroni WJr, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, Azevedo JL. 2001. Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229-236.
 
[57]  Fisher PJ, Petrini O, Scott HML. 1992. The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol 122:299-305.
 
[58]  Brooks DS, Gonzales CF, Appel DN, Filer, TH. 1994. Evaluation of endophytic bacteria as potential biological control agents for oak wilt. Biol Control 4:373-381.
 
[59]  Mahaffe WF, Kloepper JW, van Vuurde JWL, van der Wolf JM, van der Brink M. 1997. Endophytic colonization of Phaseolus valgaris by Pseudomonas fluorescens strain 89b-27 and Enterobacter asburiae strain JM22, p 180. In: Improving plant productivity in rhizosphere bacteria (Ryder MH; Stephens PM; Bowen GD), CSIRO Melbourne, Australis.
 
[60]  Ferreira A, Quecine AC, Lacava PT, Oda S, Azevedo JL, Araujo WL. 2008. Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomera. FEMS Microbiol Lett 287:8-14.
 
[61]  Sturz AV, Christie BR, Matheson BG, Nowak J. 1997. Biodiversity of endophytic bacteria which colonize red clover nodules; roots; stems and foliage and their influence on host growth. Biol Fertil Soils 25:13-19.
 
[62]  Sandhiya GS, Sugitha TC, Balachandar D, Kumar K. 2005. Endophytic colonization and in planta nitrogen fixation by a diazotrophic Serratia sp. in rice. Indian J Exp Biol 43:802-807.
 
[63]  Quadt-Hallmann A, Kloepper JW. 1996. Immunological detection and localization of the cotton endophyte Enterobacter asburiae JM22 in different plant species. Can J Microbiol 42:1144-1154.
 
[64]  Vega FE, Pava-Ripoll M, Posada F, Buyer JS. 2005. Endophytic bacteria in Coffea arabica L. J Basic Microbiol 45:371-380.
 
[65]  Wang ET, Tan Y, Guo XW, Rodriguez-Duran R, Boll G, Martínez Romero E. 2006. Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch Microbiol 186:251-259.
 
[66]  Li JH, Wang ET, Chen WF, Chen WX. 2008. Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in eilongjiang province of China. Soil Biol Biochem 40:238-246.
 
[67]  Torres AR, Araújo WL, Cursino L, Hungria M, Plotegher F, Mostasso FL, Azevedo JL. 2008. Diversity of endophytic Enterobacteria associated with different host plants. J Microbiol 46:373-379.
 
[68]  Chelius MK, Triplett EW. 2001. The diversity of Archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252-263.
 
[69]  Kaiser O, Pühler A, Selbitschka W. 2001. Phylogenetic analysis of microbial diversity in the rhizoplane of oilseed rape (Brassica napus cv. Westar) employing cultivation-dependent and cultivation- independent approaches. Microb Ecol 42:136-149.
 
[70]  Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A. 2004. Bacterial communities associated with flowering plants of the Ni hyper accumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667-2677.
 
[71]  Araujo WL, Marcon J, Maccheroni W, Van Elsas JJD, Van Vuurde JWL, Azevedo JL. 2002. Diversity of Endophytic Bacterial Populations and Their Interaction with Xylella fastidiosa in Citrus Plants. Appl Enviro Microbiol 68:4906-4914.
 
[72]  Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W. 2008. Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microbial Ecology 55: 415-24.
 
[73]  Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK. 2002. Isolation and Characterization of Endophytic Colonizing Bacteria from Agronomic Crops and Prairie Plants. Appl Environ Microbiol 68:2198-2208.
 
[74]  Conn VM, Franco CM. 2004. Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl Environ Microbiol 70: 1787-1794.
 
[75]  Rijavec T, Lapanje A, Dermastia M, Rupnik M. 2007. Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802-808.
 
[76]  Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244-125.
 
[77]  Mocali S, Bertelli E, Cello F, Mengoni A, Sfalanga A, Viliani F, Caciotti A, Tegli S, Surico G, Fani R. 2003. Fluctuation of bacteria isolated from elm tissues during different seasons and from different plants organs. Res Microbiol 154:105-114.
 
[78]  Dalmastri C, Chiarini L, Cantale C, Bevivino A, Tabacchiono S. 1999. Soil type and maize cultivar affect the genetic diversity of maize root associated Burkholderia cepacia populations. Microb Ecol 38:273-284.
 
[79]  Lemanceau P, Samson R, Alabouvette C. 1988. Recherches sur la résistance des sols aux maladies. XV. Comparaison des populations de Pseudomonas fluorescens dans un sol résistant et un sol sensible aux fusarioses vasculaires. Agronomie 8:243-249.
 
[80]  Sedra MyH. 1985. Potentiel infectieux et réceptivité de quelques sols de palmeraies à la fusariose vasculaire du palmier dattier (bayoud) causée par Fusarium oxysporum f.sp. albedinis (Kill. et Maire) Malencon, p 88. Thèse de troisième cycle. Agronomie, I.A.V. Hassan II, Rabat.
 
[81]  Sedra MyH, Maslouhy MyA. 1995. La fusariose vasculaire du palmier dattier (Bayoud). II. Action inhibitrice des filtrats de culture de six microorganismes antagonistes isolés des sols de la palmeraie de Marrakech sur le développement in vitro de Fusarium oxysporum f. sp. Albedinis. Al Awamia 90:1-8.
 
[82]  Zhang S, Thomas LW, Miriam CM, John AM, Joseph WK, Waldemar K. 2010. Evaluation of plant growth-promoting Rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol Control 53:129-135.
 
[83]  Das IK, Indira S, Annapurna A, Seetharama N. 2008. Biocontrol of charcoal rot in sorghum by fluorescent pseudomonads associated with the rhizosphere. Crop Prot 27:1407-1414.
 
[84]  Carrim AJI, Barbosa EC, Vieira JDG. 2006. Enzymatic activity of endophytic bacterial isolates of jacaranda decurrens cham. (Carobinha-do-campo). Braz Arch Biol Technol 49:353-359.
 
[85]  Reinhold-Hurek B, Hurek T. 1998. Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139-144.
 
[86]  Beckord LD, Kneen E, Lewis KH. 1945. Bacterial amylases. Production on wheat bran. Industrial and Engineering Chemistry 37: 692-696.
 
[87]  Schmidt J, John M. 1979. Starch metabolism in Pseudomonas stuteri. I. Studies on matotetraose forming amylase. Biochim Biophys Acta Enzymol 566:88-99.
 
[88]  Ahmadzadeh M, Tehrani AS. 2009. Evaluation of fluorescent Pseudomonas for plant growth promotion, antifungal activity against Rhizoctonia solani on common bean and biocontrol potential. Biol Control 48:101-107.
 
[89]  Ait Barka E, Gognies S, Nowak J, Audran JC, Belarbi A. 2002. Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth,” Biol Control 24: 135-142.
 
[90]  Gorlach-Lira K, Stefaniak O. 2009. Antagonistic Activity of Bacteria Isolated from Crops Cultivated in a Rotation System and a Monoculture against Pythium debaryanum and Fusarium oxysporum. Folia Microbiol 54:447-450.
 
[91]  Feurer C. 2004. Caractérisation de la biodiversité des bactéries coryneformes dans les fromages à croûte lavée, p 183. Approche de leurs effets antagonistes contre les pathogènes alimentaires et en particulier Listeria monocytogenes, PhD thesis, National Agronomic Institute, Paris.
 
[92]  Monnet C, Loux V, Gibrat JF, Spinnler E, Barbe V, Vacherie B, Gavory F, Gourbeyre E, Siguier P, Chandler M, Elleuch R, Irlinger F, Vallaeys T. 2010. The Arthrobacter arilaitensis Re117 Genome Sequence reveals its Genetic Adaptation to the Surface of Cheese. PLoS One 24:154-89.
 
[93]  Audus LJ. 1950. Biological detoxification of 2, 4-dichlorophenoxyacetic acid in soils: isolation of an effective organism. Nature 166:365-67.
 
[94]  Strong LC, Rosendahl C, Johson G, Sadowsky MJ, Wackett LP. 2002. Arthrobacter aurescens TC1 metabolizes diverse s-triazine ring compounds. Appl Environ Microbiol 68: 5973-80.
 
[95]  Nakatsu CH, Carmosini N, Baldwin B, Beasley F, Kourtev P, Konopka A. 2005. Soil Microbial Community Responses to Additions of Organic Carbon Substrates and Heavy Metals (Pb and Cr). Appl Environ Microbiol 71:7679-7689.
 
[96]  Jeun YC, Park KS, Kim CH, Fowler WD, Kloepper JW. 2004. Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biol Control 29:34-42.