Antonie van Leeuwenhoek

, Volume 112, Issue 1, pp 75–90 | Cite as

The plant-growth-promoting actinobacteria of the genus Nocardia induces root nodule formation in Casuarina glauca

  • Faten Ghodhbane-Gtari
  • Imen Nouioui
  • Karima Hezbri
  • Emily Lundstedt
  • Timothy D’Angelo
  • Zakkary McNutt
  • Laurent Laplaze
  • Hassen Gherbi
  • Virginie Vaissayre
  • Sergio Svistoonoff
  • Hela ben Ahmed
  • Abdelatif Boudabous
  • Louis S. TisaEmail author
Original Paper


Actinorhizal plants form a symbiotic association with the nitrogen-fixing actinobacteria Frankia. These plants have important economic and ecological benefits including land reclamation, soil stabilization, and reforestation. Recently, many non-Frankia actinobacteria have been isolated from actinorhizal root nodules suggesting that they might contribute to nodulation. Two Nocardia strains, BMG51109 and BMG111209, were isolated from Casuarina glauca nodules, and they induced root nodule-like structures in original host plant promoting seedling growth. The formed root nodule-like structures lacked a nodular root at the apex, were not capable of reducing nitrogen and had their cortical cells occupied with rod-shaped Nocardiae cells. Both Nocardia strains induced root hair deformation on the host plant. BMG111209 strain induced the expression of the ProCgNin:Gus gene, a plant gene involved in the early steps of the infection process and nodulation development. Nocardia strain BMG51109 produced three types of auxins (Indole-3-acetic acid [IAA], Indole-3-Byturic Acid [IBA] and Phenyl Acetic Acid [PAA]), while Nocardia BMG111209 only produced IAA. Analysis of the Nocardia genomes identified several important predicted biosynthetic gene clusters for plant phytohormones, secondary metabolites, and novel natural products. Co-infection studies showed that Nocardia strain BMG51109 plays a role as a “helper bacteria” promoting an earlier onset of nodulation. This study raises many questions on the ecological significance and functionality of Nocardia bacteria in actinorhizal symbioses.


Non-Frankia actinobacteria Nocardia Plant infectivity Auxins Actinorhizal symbiosis Plant-growth-promotion 



This work was supported in part by CMCU (Comité Mixte Tuniso-Français pour la Coopération inter-Universitaire no 09G0916 to MG and LL) and the Agence Nationale de la Recherche (Grant ANR-08-JCJC-0070-01 to LL). FG-G was supported in part by the Visiting Scientist and Postdoctoral Scientist Program administered by the NH AES at the University of New Hampshire. This work was also supported by the USDA National Institute of Food and Agriculture Hatch 022821 (LST), Agriculture and Food Research Initiative Grant 2015-67014-22849 from the USDA National Institute of Food and Agriculture (LST), and the College of Life Science and Agriculture at the University of New Hampshire-Durham. A Summer Undergraduate Research Fellowship (SURF) from the University of New Hampshire-Durham supported EL. Partial funding was provided by the New Hampshire Agricultural Experiment Station. This is Scientific Contribution Number 2786.

Authors Contribution

FGG, LL, AB and LST conceived the study. FGG, IN, EL, TD, ZM, HK, VV, and HG performed the research. EL, TD, IN, FGG, and LST analysed the data. FGG, and LST wrote the manuscript. All the authors approved the paper.

Compliance with ethical standards

Conflict of interest

The authors have declared that they have no competing interest exists.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10482_2018_1147_MOESM1_ESM.pdf (28 kb)
Supplementary material 1 (PDF 28 kb)
10482_2018_1147_MOESM2_ESM.pdf (75 kb)
Supplementary material 2 (PDF 74 kb)
10482_2018_1147_MOESM3_ESM.pdf (123 kb)
Supplementary material 3 (PDF 122 kb)
10482_2018_1147_MOESM4_ESM.pdf (42 kb)
Supplementary material 4 (PDF 42 kb)
10482_2018_1147_MOESM5_ESM.pdf (43 kb)
Supplementary material 5 (PDF 42 kb)
10482_2018_1147_MOESM6_ESM.pdf (100 kb)
Supplementary material 6 (PDF 99 kb)
10482_2018_1147_MOESM7_ESM.pdf (121 kb)
Supplementary material 7 (PDF 120 kb)
10482_2018_1147_MOESM8_ESM.pdf (102 kb)
Supplementary material 8 (PDF 102 kb)
10482_2018_1147_MOESM9_ESM.pdf (126 kb)
Supplementary material 9 (PDF 125 kb)


  1. Alonso-Vega P, Normand P, Bacigalupe R, Pujic P, Lajus A, Vallenet D, Carro L, Coll P, Trujillo ME (2012) Genome sequence of Micromonospora lupini Lupac 08, isolated from root nodules of Lupinus angustifolius. J Bacteriol 194:4135CrossRefGoogle Scholar
  2. Aserse AA, Rasanen LA, Aseffa F, Hailemariam A, Lindstrom K (2013) Diversity of sporadic symbionts and nonsymbiotic endophytic bacteria isolated from nodules of woody, shrub, and food legumes in Ethiopia. Appl Microbiol Biotech 97:10117–10134CrossRefGoogle Scholar
  3. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  4. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Stevens RL, Vonstein V, Xia F (2012) SEED servers: high-performance access to the SEED genomes, annotations, and metabolic models. PLoS ONE 7:e48053CrossRefGoogle Scholar
  5. Baker D, Okeefe D (1984) A modified sucrose fractionation procedure for the isolation of frankiae from actinorhizal root-nodules and soil samples. Plant Soil 78:23–28. CrossRefGoogle Scholar
  6. Beauchemin NJ, Furnholm T, Lavenus J, Svistoonoff S, Doumas P, Bogusz D, Laplaze L, Tisa LS (2012) Casuarina root exudates alter Frankia physiology, surface properities and plant infectivity. Appl Environ Microbiol 78:575–580. CrossRefGoogle Scholar
  7. Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319Google Scholar
  8. Benson DR, Brooks JM, Huang Y, Bickhart DM, Mastronunzio JE (2011) The biology of Frankia sp. strains in the post-genome era. Mol Plant Microbe Interact 24:1310–1316CrossRefGoogle Scholar
  9. Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43CrossRefGoogle Scholar
  10. Berry AM, Torrey JG (1983) Root hair deformation in the infection process of Alnus rubra. Can J Bot 61:2863–2876CrossRefGoogle Scholar
  11. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T (2013) antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41:W204–W212CrossRefGoogle Scholar
  12. Blin K, Wolf T, Chevrette MG, Lu XW, Schwalen CJ, Kautsar SA, Duran HGS, Santos ELCDL, Kim Hu, Nave M, Dickschat JS, Mitchell DA, Shelest E, Breitling R, Takano E, Lee SY, Weber T, Medema MH (2017) antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 45:W36–W41. CrossRefGoogle Scholar
  13. Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 25:1075–1080CrossRefGoogle Scholar
  14. Carro L, Pujic P, Trujillo ME, Normand P (2013) Micromonospora is a normal occupant of actinorhizal nodules. J Biosci 38:685–693CrossRefGoogle Scholar
  15. Champion A, Lucas M, Tromas A, Vaissayre V, Crabos A, Diedhiou I, Prodjinoto H, Moukouanga D, Pirolles E, Cissoko M, Bonneau J, Gherbi H, Franche C, Hocher V, Svistoonoff S, Laplaze L (2015) Inhibition of auxin signaling in Frankia species-infected cells in Casuarina glauca nodules leads to increased nodulation. Plant Physiol 167(3):1149–1157. CrossRefGoogle Scholar
  16. Clavijo F, Diedhiou I, Vaissayre V, Acolatse J, Moukouanga D, Crabos A, Auguy F, Franche C, Gherbi H, Champion A, Hocher V, Bogusz D, Tisa LS, Svistoonhoff S (2015) The Casuarina NIN gene is a transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytol 208:887–903. CrossRefGoogle Scholar
  17. Diagne N, Arumugam K, Ngom M, Nambiar-Veetil M, Franche C, Narayanan KK, Laplaze L (2013a) Use of Frankia and actinorhizal plants for degraded lands reclamation. Biomed Res Int 2013:948258. CrossRefGoogle Scholar
  18. Diagne N, Diouf D, Svistoonoff S, Kane A, Noba K, Franche C, Bogusz D, Duponnois R (2013b) Casuarina in Africa: distribution, role and importance of arbuscular mycorrhizal, ectomycorrhizal fungi and Frankia on plant development. J Environ Manag 128:204–209. CrossRefGoogle Scholar
  19. Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microbiol 52:248–260CrossRefGoogle Scholar
  20. Felsentein J (1985) Confidence limits on phylogeny: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  21. Ghodhbane-Gtari F, Tisa LS (2014) Ecology and physiology of non-Frankia actinobacteria from actinorhizal plants. In: Katsy EI (ed) Plasticity in plant-growth-promoting and phytopathogenic bacteria. Springer, New York, pp 27–42CrossRefGoogle Scholar
  22. Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Chouia B, Jaouani A, Boudabous A, Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57CrossRefGoogle Scholar
  23. Ghodhbane-Gtari F, Nouioui I, Salem K, Ktari A, del Carmen Montero-Calasanz M, Tisa LS, Klenk H-P, Gtari M (2014) Nocardia casuarinae sp. nov., an actinobacterial endophyte isolated from root nodules of Casuarina glauca. Antonie Van Leeuwenhoek 105(6):1099–1106CrossRefGoogle Scholar
  24. Ghodhbane-Gtari F, Beauchemin N, Gueddou A, Hezbri K, Ktari A, Louati M, Nouioui I, Chen A, Huntemann M, Ivanova N, Kyrpides N, Markowitz V, Mavrommatis K, Pagani I, Sen A, Wall L, Woyke T, Gtari M, Tisa LS (2016a) Permanent improved high quality draft genome sequence of Nocardia casuarinae strain BMG51109 an endophyte of actinorhizal root nodules of Casuarina glauca. Genome Announc 4(4):e00799-16. CrossRefGoogle Scholar
  25. Ghodhbane-Gtari F, Beauchemin N, Gueddou A, Hezbri K, Ktari A, Louati M, Nouioui I, Chen A, Huntemann M, Ivanova N, Kyrpides N, Markowitz V, Mavrommatis K, Pagani I, Sen A, Wall L, Woyke T, Gtari M, Tisa LS (2016b) Permanent draft genome sequence of Nocardia sp. BMG111209, an actinobacterium isolated from nodules of Casuarina glauca. Genome Announc 4(4):e00770-16. CrossRefGoogle Scholar
  26. Gourion B, Berrabah F, Ratet P, Stacey G (2014) Rhizobium–legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20(3):186–194CrossRefGoogle Scholar
  27. Gtari M, Brusetti L, Gharbi S, Diego M, Boudabous A, Daffonchio D (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 234:349–355CrossRefGoogle Scholar
  28. Gtari M, Brusetti L, Hassen A, Mora D, Daffonchio D, Boudabous A (2007) Genetic diversity among Elaeagnus compatible Frankia strains and sympatric related nitrogen fixing actinobacteria revealed by nifH sequence analysis. Soil Biol Biochem 39:372–377CrossRefGoogle Scholar
  29. Hirsch AM, Alvarado J, Bruce D, Chertkov O, De Hoff PL, Detter JC, Fujishigea NA, Goodwind LA, Hand J, Hanc S, Ivanovac N, Lande ML, Luma MR, Milani-Nejada N, Nolane M, Patic A, Pitluckd S, Trana SS, Woyke T, Valdés M (2013) Complete genome sequence of Micromonospora strain L5, a potential plant-growth-regulating actinomycete, originally isolated from Casuarina equisetifolia root nodules. Genome Announc 1(5):e00759-13CrossRefGoogle Scholar
  30. Hurek T, Handley LL, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant Microbe Interact 15(3):233–242CrossRefGoogle Scholar
  31. Jukes TH, Cantor CR (1969) Evolution of protein molecules. Academic Press, New York, pp 21–132Google Scholar
  32. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30CrossRefGoogle Scholar
  33. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721CrossRefGoogle Scholar
  34. Knowlton S, Dawson JO (1983) Effects of Pseudomonas cepacia and cultural factors on the nodulation of Alnus rubra Roots by Frankia. Can J Bot 61(11):2877–2882CrossRefGoogle Scholar
  35. Knowlton S, Berry A, Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can J Microbiol 26(8):971–977CrossRefGoogle Scholar
  36. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWillam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefGoogle Scholar
  37. Lerat E, Daubin V, Ochman H, Moran N (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:807–813CrossRefGoogle Scholar
  38. Markowitz VM, Korzeniewski F, Palaniappan K, Szeto E, Werner G, Padki A, Zhao XL, Dubchak I, Hugenholtz P, Anderson I, Lykidis A, Mavromatis K, Ivanova N, Kyrpides NC (2006) The integrated microbial genomes (IMG) system. Nucleic Acids Res 34:D344–D348CrossRefGoogle Scholar
  39. Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC (2009) IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25:2271–2278. CrossRefGoogle Scholar
  40. Merzaeva OV, Shirokikh IG (2010) The production of auxins by the endophytic bacteria of winter rye. Appl Biochem Microbiol 46(1):44–50CrossRefGoogle Scholar
  41. Mine A, Sato M, Tsuda K (2014) Toward a systems understanding of plant–microbe interactions. Frontiers Plant Sci 5:423CrossRefGoogle Scholar
  42. Ngom M, Oshone R, Diagne N, Cissoko M, Svistoonoff S, Tisa LS, Laplaze L, Sy MO, Champion A (2016) Tolerance to environmental stress by the nitrogen-fixing actinobacterium Frankia and its role in actinorhizal plants adaptation. Symbiosis 70:17–29. CrossRefGoogle Scholar
  43. Niemann J, Tisa LS (2008) Nitric oxide and oxygen regulate truncated hemoglobin gene expression in Frankia strain CcI3. J Bacteriol 190:7864–7867. CrossRefGoogle Scholar
  44. Niner BM, Brandt JP, Villegas MC, Marshall CR, Hirsch AM, Valdes M (1996) Analysis of partial sequences of genes coding for 16S rRNA of actinomycetes isolated from Casuarina equisetifolia nodules in Mexico. Appl Environ Microbiol 62:3034–3036Google Scholar
  45. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz NC, Göker M, Meier-Kolthoff JP, Schumann P, Rohde M, Goodfellow M, Fernandez MP, Normand P, Tisa LS, Klenk H-P, Gtari M (2016) Proposal of a type strain for Frankia alni (Woronin 1866), and recognition Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov. Int J Syst Evol Microbiol 66:5201–5210. CrossRefGoogle Scholar
  46. Patten CL, Glick BR (1996) Bacterial biosynthesis on indole-3-acetic acid. Can J Microbiol 42:207–220CrossRefGoogle Scholar
  47. Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of host plant root system. Appl Environ Microbiol 68:3795–3801CrossRefGoogle Scholar
  48. Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin N, Band L, Chopard J, Crabos A, Conejero G, Peret B, Verdeil J-L, Hocher V, Franche C, Bennett MJ, Tisa LS, Lalpaze L (2010) Specific auxin carriers localization direct auxin accumulation in plants cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiol 154:1372–1380.
  49. Ramirez-Saad H, Janse JD, Akkermans ADL (1998) Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod–/Fix–actinomycete. Can J Microbiol 44:140–148CrossRefGoogle Scholar
  50. Ridgway KP, Marland LA, Harrison AF, Wright J, Young JPW, Fitter AH (2004) Molecular diversity of Frankia in root nodules of Alnus incana grown with inoculum from polluted urban soils. FEMS Microbiol Ecol 50:255–263. CrossRefGoogle Scholar
  51. Ritchie NJ, Myrold DD (1999) Geographic distribution and genetic diversity of Ceanothus-infective Frankia strains. Appl Environ Microb 65(4):1378–1383Google Scholar
  52. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278(1):1–9CrossRefGoogle Scholar
  53. Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  54. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C-T method. Nat Protoc 3:1101–1108CrossRefGoogle Scholar
  55. Solans M (2007) Discaria trinervisFrankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250CrossRefGoogle Scholar
  56. Solans M, Vobis G (2003) Actinomycetes saprofiticos asociados a la rizosfera rizoplano de Discaria trinervis. Ecologia Austral 13:97–107Google Scholar
  57. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448CrossRefGoogle Scholar
  58. Svistoonoff S, Laplaze L, Auguy F, Runions J, Duponnois R, Haseloff J, Franche C, Bogusz D (2003) cg12 expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development. Mol Plant Microbe Interact 16:600–607CrossRefGoogle Scholar
  59. Svistoonoff S, Sy MO, Diagne N, Barker DG, Bogusz D, Franche C (2010) Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Mol Plant Microbe Interact 23:740–747CrossRefGoogle Scholar
  60. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. CrossRefGoogle Scholar
  61. Tisa L, Mcbride M, Ensign JC (1983) Studies of Growth and Morphology of Frankia Strains EAN1pec, EuI1c, CpI1, and ACN1ag. Can J Bot 61:2768–2773CrossRefGoogle Scholar
  62. Tisa LS, Chval MS, Krumholz GD, Richards J (1999) Antibiotic resistance patterns of Frankia strains. Can J Bot 77:1257–1260Google Scholar
  63. Trujillo ME, Kroppenstedt RE, Schumann P, Carro L, Martinez-Molina E (2006) Micromonospora coriariae sp. nov., isolated from root nodules of Coriaria myrtifolia. Int J Syst Evol Microbiol 56:2381–2385CrossRefGoogle Scholar
  64. Trujillo ME, Riesco R, Benito P, Carro L (2015) Endophytic actinobacteria and the interaction of Micromonospora and nitrogen fixing plants. Front Microbiol 6:1341. CrossRefGoogle Scholar
  65. Tsukamura M (1982) Numerical analysis of the taxonomy of nocardiae and rhodococci. Division of Nocardia asteroides sensu stricto into two species and descriptions of Nocardia paratuberculosis sp. nov. Tsukamura (formerly the Kyoto-I group of Tsukamura), Nocardia nova sp. nov. Tsukamura, Rhodococcus aichiensis sp. nov., Tsukamura, Rhodococcus chubuensis sp. nov., Tsukamura, and Rhodococcus obuensis sp. nov. Tsukamura. Microbiol Immunol 26:1101–1119CrossRefGoogle Scholar
  66. Valdés M, Pérez NM, de los Santo PE, Mellado JC, Cabrielas JJP, Normand P, Hirsh M (2004) Non-Frankia actinomycetes isolated from surface sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466CrossRefGoogle Scholar
  67. Valdés D, Huss-Danell K, Lavire C, Normand P, Wall L (2006) Further characterization of new symbiotic nitrogen fixing non-Frankia actiomycetes isolated from nodules of Alnus acuminata. In: The 14th international meeting on Frankia and actinorhizal plants. Department of Plant Physiology, UPSC, Umea University, UmeaGoogle Scholar
  68. Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36:1251–1275CrossRefGoogle Scholar
  69. Zhang Z, Lopez MF, Torrey JG (1984) A comparison of cultural-characteristics and infectivity of Frankia isolates from root-nodules of casuarina species. Plant Soil 78:79–90. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Faten Ghodhbane-Gtari
    • 1
  • Imen Nouioui
    • 1
  • Karima Hezbri
    • 1
  • Emily Lundstedt
    • 2
  • Timothy D’Angelo
    • 2
  • Zakkary McNutt
    • 2
  • Laurent Laplaze
    • 3
    • 4
    • 5
  • Hassen Gherbi
    • 3
  • Virginie Vaissayre
    • 6
  • Sergio Svistoonoff
    • 3
    • 4
    • 5
  • Hela ben Ahmed
    • 7
  • Abdelatif Boudabous
    • 1
  • Louis S. Tisa
    • 2
    Email author
  1. 1.Laboratoire Microorganismes et Biomolécules ActivesUniversité Tunis El Manar (FST) & Université Carthage (INSAT)TunisTunisia
  2. 2.Department of Molecular, Cellular, and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.LSTM, UMR 040 IRD/INRA/CIRAD/ Université Montpellier/Supagro, TA A-82/J, Campus International de BaillarguetMontpellierFrance
  4. 4.LCM, IRD/ISRA/UCAD, Centre de Recherche de Bel AirDakarSenegal
  5. 5.LMI LAPSE, Centre de Recherche de Bel AirDakarSenegal
  6. 6.ECOBIOFrench National Research Institute for Sustainable Development (IRD)MontpellierFrance
  7. 7.Unité d’Ecophysiologie et Nutrition des plantes, Département de Biologie, Faculté des Sciences de TunisTunisTunisia

Personalised recommendations