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Symbiotic Performance of Diverse Frankia Strains on Salt- Stressed Casuarina Glauca and Casuarina Equisetifolia Plants

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Symbiotic Performance of Diverse Frankia Strains on Salt- Stressed Casuarina Glauca and Casuarina Equisetifolia Plants University of New Hampshire University of New Hampshire Scholars' Repository Molecular, Cellular and Biomedical Sciences Scholarship Molecular, Cellular and Biomedical Sciences 8-31-2016 Symbiotic Performance of Diverse Frankia Strains on Salt- Stressed Casuarina glauca and Casuarina equisetifolia Plants Mariama Ngom Centre de Recherche de Bel-Air Krystelle Gray Centre de Recherche de Bel-Air Nathalie Diagne Centre de Recherche de Bel-Air Rediet Oshone University of New Hampshire, Durham Joel Fardoux Institut de Recherche pour le Développement See next page for additional authors Follow this and additional works at: https://scholars.unh.edu/mcbs_facpub Recommended Citation Ngom, M., K. Gray, N. Diagne, R. Oshone, J. Fardoux, H. Gherbi, V. Hocher, S. Svistoonoff, L. Laplaze, L. S. Tisa, M. O. Sy and A. Champion. 2016. Symbiotic performance of diverse Frankia strains on salt-stressed Casuarina glauca and Casuarina equisetifolia plants. Frontier in Plant Sciences. 7:1331. doi: 10.3389/ fpls.2016.01331 This Article is brought to you for free and open access by the Molecular, Cellular and Biomedical Sciences at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Molecular, Cellular and Biomedical Sciences Scholarship by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. Authors Mariama Ngom, Krystelle Gray, Nathalie Diagne, Rediet Oshone, Joel Fardoux, Hassen Gherbi, Valerie Hocher, Sergio Svistoonoff, Laurent Laplaze, Louis S. Tisa, Mame Oureye Sy, and Antony Champion This article is available at University of New Hampshire Scholars' Repository: https://scholars.unh.edu/mcbs_facpub/ 179 ORIGINAL RESEARCH published: 31 August 2016 doi: 10.3389/fpls.2016.01331 Symbiotic Performance of Diverse Frankia Strains on Salt-Stressed Casuarina glauca and Casuarina equisetifolia Plants Mariama Ngom 1, 2, 3, Krystelle Gray 1, 3, 4, Nathalie Diagne 1, 5, Rediet Oshone 6, Joel Fardoux 7, Hassen Gherbi 7, Valérie Hocher 7, Sergio Svistoonoff 1, 3, 7, Laurent Laplaze 1, 3, 4, Louis S. Tisa 6, Mame O. Sy 1, 2 and Antony Champion 1, 4* 1 Laboratoire Mixte International Adaptation des Plantes et microorganismes associés aux Stress Environnementaux, Centre de Recherche de Bel-Air, Dakar, Sénégal, 2 Laboratoire Campus de Biotechnologies Végétales, Département de Biologie Végétale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop, Dakar, Sénégal, 3 Laboratoire Commun de Microbiologie Institut de Recherche pour le Développement/Institut Sénégalais de Recherches Agricoles/Université Cheikh Anta Diop, Centre de Recherche de Bel-Air, Dakar, Sénégal, 4 UMR DIADE, Institut de Recherche pour le Développement, 5 Edited by: Montpellier, France, Centre National de Recherches Agronomiques, Institut Sénégalais de Recherches Agricoles, Bambey, 6 Vasileios Fotopoulos, Sénégal, Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, NH, USA, 7 Cyprus University of Technology, Laboratoire des Symbioses Tropicales et Méditerranéennes, Institut de Recherche pour le Développement/INRA/CIRAD/ Cyprus Université Montpellier/Sup agro, Montpellier, France Reviewed by: Raffaella Balestrini, Symbiotic nitrogen-fixing associations between Casuarina trees and the actinobacteria National Research Council, Italy Frankia are widely used in agroforestry in particular for salinized land reclamation. The aim Anandham Rangasamy, Tamil Nadu Agricultural University, of this study was to analyze the effects of salinity on the establishment of the actinorhizal India symbiosis between C. glauca and two contrasting Frankia strains (salt sensitive; CcI3 vs. *Correspondence: salt tolerant; CeD) and the role of these isolates in the salt tolerance of C. glauca and C. Antony Champion [email protected] equisetifolia plants. We show that the number of root nodules decreased with increasing salinity levels in both plants inoculated with CcI3 and CeD. Nodule formation did not Specialty section: occur in seedlings inoculated with CcI3 and CeD, at NaCl concentrations above 100 This article was submitted to Crop Science and Horticulture, and 200 mM, respectively. Salinity also affected the early deformation of plant root hairs a section of the journal and reduced their number and size. In addition, expression of symbiotic marker Cg12 Frontiers in Plant Science gene, which codes for a subtilase, was reduced at 50 mM NaCl. These data suggest Received: 14 May 2016 that the reduction of nodulation in C. glauca under salt stress is in part due to inhibition Accepted: 18 August 2016 Published: 31 August 2016 of early mechanisms of infection. We also show that prior inoculation of C. glauca and Citation: C. equisetifolia with Frankia strains CcI3 and CeD significantly improved plant height, Ngom M, Gray K, Diagne N, dry biomass, chlorophyll and proline contents at all levels of salinity tested, depending Oshone R, Fardoux J, Gherbi H, Casuarina-Frankia in vitro Hocher V, Svistoonoff S, Laplaze L, on the association. There was no correlation between salt Tisa LS, Sy MO and Champion A tolerance of Frankia strains and efficiency in planta under salt-stressed conditions. Our (2016) Symbiotic Performance of results strongly indicate that increased N nutrition, photosynthesis potential and proline Diverse Frankia Strains on Salt-Stressed Casuarina glauca and accumulation are important factors responsible for salt tolerance of nodulated C. glauca Casuarina equisetifolia Plants. and C. equisetifolia. Front. Plant Sci. 7:1331. doi: 10.3389/fpls.2016.01331 Keywords: salinity, Frankia, Casuarina glauca, Casuarina equisetifolia, root hair deformation, CgNIN, Cg12, proline Frontiers in Plant Science | www.frontiersin.org 1 August 2016 | Volume 7 | Article 1331 Ngom et al. Actinorhizal Symbiosis and Salt-Stressed Response INTRODUCTION the host plant through a deformed root hair (Franche et al., 1998) and induce the expression of several plant genes involved Soil salinization is a major problem worldwide. Indeed, high in actinorhizal nodule formation and functioning. Among them levels of salt in soil limit crop production and increase the loss are the CgNIN, encoding a transcriptional factor, expressed at of arable land. More than 800 million hectares of land worldwide pre-infection stages in root hairs competent for Frankia infection are salt-affected (Munns and Tester, 2008). By the year 2050, (Clavijo et al., 2015) and Cg12, encoding a subtilase, whose 50% of all arable lands could be affected by salinity (Wang et al., expression is linked to the infection of root hairs and cortical cells 2003). There is therefore a need to design strategies to rehabilitate by Frankia (Laplaze et al., 2000; Svistoonoff et al., 2003). salinized areas. Frankia is a genus of soil actinobacteria (Normand et al., Actinorhizal plants belonging to Casuarinaceae family such 2014). These Gram+, aerobic, heterotrophic bacteria are able as Casuarina glauca and C. equisetifolia are able to grow to fix nitrogen both under free-living conditions and inside under saline environments (El-Lakany and Luard, 1983; Girgis symbiotic root nodule (Simonet et al., 1989). The first pure et al., 1992; Tani and Sasakawa, 2003). They are fast- culture of a Frankia strain was isolated from Comptonia peregrina growing trees, originated from Australia and Pacific islands, nodules (Callaham et al., 1978). Since then, several Frankia widely used in agroforestry systems for several purposes strains have been isolated from different actinorhizal species (Diem and Dommergues, 1990). In many tropical and sub- (Diem et al., 1982, 1983; Gomaa et al., 2008; Gtari et al., tropical countries, Casuarina species play a major role in 2015). They are grouped into four major clusters (Normand land reclamation, crop protection and as windbreaks (National et al., 1996). Frankia strains in cluster 1 form nodules either Research Council, 1984). In Senegal, a green barrier of with members of Betulaceae and Myricaceae (cluster 1a) or C. equisetifolia was established on the northern Atlantic fringe Casuarinaceae (cluster 1c). Cluster 2 includes Frankia strains able between Dakar and Saint-Louis to stabilize sand dunes and to infect the Coriariaceae, Datiscaceae, Rosaceae, and Ceanothus protect the vegetable and fruit producing so-called “Niayes” of the Rhamnaceae. Frankia strains in cluster 3 form effective area (Maheut and Dommergues, 1961; Mailly et al., 1994). nodules with the Myricaceae, Rhamnaceae, Elaeagnaceae, and C. equisetifolia is also appreciated for source of poles, firewood Gymnostoma belonging to Casuarinaceae. Cluster 4 includes and charcoal (Diagne et al., 2013; Potgieter et al., 2014). Thus, atypical Frankia strains, which are non-infective and/or non- this family of plants is of high importance for salinized land nitrogen-fixing. Casuarina isolates show contrasting responses in reclamation. their salt tolerance (Ngom et al., 2016). Indeed, some strains are Casuarina species are pioneer plants, able to colonize more tolerant in vitro to salt stress than others even though they poor and degraded lands and increase their fertility (Duhoux were isolated from the same host plant (Dawson and Gibson, and Franche, 2003). Therefore, they promote development of 1987; Fauzia, 1999; Tani and Sasakawa, 2003; Oshone et al., pedogenetic processes leading to the formation of a more 2013). Nevertheless, the symbiotic performance under salt stress suitable microclimate for the installation of other plants
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