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Role of Auxin During Intercellular Infection of Discaria Trinervis By Role of auxin during intercellular infection of Discaria trinervis by Frankia Leandro Imanishi, Francine Manuelle Perrine-Walker, Adama Ndour, Alice Vayssieres, Geneviève Conejero, Mikael Lucas, Antony Champion, Laurent Laplaze, Luis Wall, Sergio Svistoonoff To cite this version: Leandro Imanishi, Francine Manuelle Perrine-Walker, Adama Ndour, Alice Vayssieres, Geneviève Conejero, et al.. Role of auxin during intercellular infection of Discaria trinervis by Frankia. Frontiers in Plant Science, Frontiers, 2014, 5, pp.399. 10.3389/fpls.2014.00399. hal-01837547 HAL Id: hal-01837547 https://hal.archives-ouvertes.fr/hal-01837547 Submitted on 27 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License ORIGINAL RESEARCH ARTICLE published: 21 August 2014 doi: 10.3389/fpls.2014.00399 Role of auxin during intercellular infection of Discaria trinervis by Frankia Leandro Imanishi 1,2, Francine M. Perrine-Walker 2, Adama Ndour 3, Alice Vayssières 2, Genevieve Conejero 4, Mikaël Lucas 2, Antony Champion 2,3, Laurent Laplaze 2,3, Luis Wall 1 and Sergio Svistoonoff 2,3* 1 Laboratorio de Bioquímica Microbiología e Interacciones Biológicas en el Suelo, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Bernal, Argentina 2 Groupe Rhizogenèse, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France 3 LAPSE and Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, Centre de Recherche de Bel-Air, Dakar, Senegal 4 Institut National de la Recherche Agronomique, Plateforme PHIV, Cirad, Montpellier, France Edited by: Nitrogen-fixing nodules induced by Frankia in the actinorhizal plant Discaria trinervis Pierre-Emmanuel Courty, University result from a primitive intercellular root invasion pathway that does not involve root hair of Basel - Botanical Institute, deformation and infection threads. Here, we analyzed the role of auxin in this intercellular Switzerland infection pathway at the molecular level and compared it with our previous work in the Reviewed by: Benoit Lacroix, State University of intracellular infected actinorhizal plant Casuarina glauca. Immunolocalisation experiments New York at Stony Brook, USA showed that auxin accumulated in Frankia-infected cells in both systems. We then Frantisek Baluska, University of characterized the expression of auxin transporters in D. trinervis nodules. No activation Bonn, Germany of the heterologous CgAUX1 promoter was detected in infected cells in D. trinervis. *Correspondence: These results were confirmed with the endogenous D. trinervis gene, DtAUX1. However, Sergio Svistoonoff, Laboratoire Commun de Microbiologie DtAUX1 was expressed in the nodule meristem. Consistently, transgenic D. trinervis IRD/ISRA/UCAD Campus de Bel-Air, plants containing the auxin response marker DR5:VENUS showed expression of the Bâtiment B3 Route des reporter gene in the meristem. Immunolocalisation experiments using an antibody against hydrocarbures, Dakar-Sénégal the auxin efflux carrier PIN1, revealed the presence of this transporter in the plasma LAPSE, BP 1386-CP 18524, Dakar, Senegal membrane of infected cells. Finally, we used in silico cellular models to analyse auxin e-mail: [email protected] fluxes in D. trinervis nodules. Our results point to the existence of divergent roles of auxin in intercellularly- and intracellularly-infected actinorhizal plants, an ancestral infection pathways leading to root nodule symbioses. Keywords: auxin, actinorrhiza, systems biology, endosymbiosis, model, AUX1, PIN, nitrogen fixation INTRODUCTION formation of nodule primordia (Roudier et al., 2003). Recently Actinorhizal symbiosis comprise more than 200 species from 8 we demonstrated that auxin also plays an important role during families distributed within the orders Fagales, Cucurbitales and actinorhizal nodule development in C. glauca.Weshowedthat Rosales, which form nitrogen fixing nodules with the soil actino- inhibition of auxin influx transport by the competitive inhibitor mycete Frankia. Unlike legumes whose nodules are characterized naphthoxyacetic acid (1-NOA) perturbs nodule formation (Péret by a peripheral vascular system, actinorhizal nodules present a et al., 2007). Auxins were detected in Frankia cultures and in central vascular bundle that structurally resembles a lateral root. Frankia-infected cells in C. glauca nodules (Perrine-Walker et al., Moreover, the actinorhizal nodule develops from the pericycle, 2010). Those infected cells were shown to express an auxin influx like lateral roots (Wall, 2000; Svistoonoff et al., 2014). carrier (CgAUX1) whereas a PIN1-like auxin efflux carrier was Auxins are involved in many developmental processes and play detected in surrounding uninfected cells (Perrine-Walker et al., a major role in lateral root initiation, differentiation and mainte- 2010). Using computer simulations we showed that the pattern of nance (Lavenus et al., 2013). Several studies revealed that auxins transporter distribution leads to auxin accumulation in infected are also involved in nodule development in legumes (Mathesius cells, where auxins possibly induce changes in gene expression, et al., 1998; De Billy et al., 2001; Pacios-Bras et al., 2003). It has cell metabolism, or in the cell wall properties (Perrine-Walker been suggested that rhizobia inhibit auxin transport at the early et al., 2010, 2011). stages of the symbiotic interaction in legumes forming indetermi- Discaria trinervis, an actinorhizal shrub belonging to the nate type of nodules (Mathesius et al., 1998; De Billy et al., 2001), Rhamnaceae family, was recently chosen as a model plant for but not in L. japonicus that forms determinate type of nodules the study of the intercellular infection pathway in actinorhizal (Pacios-Bras et al., 2003). In both cases an accumulation of auxin symbiosis (Imanishi et al., 2011). Whereas the molecular basis occurs at the site of nodule initiation and auxin is supposed to of nodulation in plants infected through root hairs has been stimulate cell divisions in the cortex and pericycle that lead to the extensively studied in Legumes and in actinorhizal plants, little www.frontiersin.org August 2014 | Volume 5 | Article 399 | 1 Imanishi et al. Discaria actinorhiza: role of auxins is known about plants infected through the intercellular infection GCAAGCCCAATTGAG-3, DtAux1_GSP1c_5 5-CTTCCTCT pathway which is found in about 75% of actinorhizal genera and GCTTGTTTCTGAGCCAACAT-3, DtAux1_GSP2c_5 5-ACG is possibly an ancestral process which led to the more sophisti- CAGCCCCAGAAAACGAAAGCCAATA-3, DtAux1_GSP1_3 5- cated root hair infection (Svistoonoff et al., 2014). The intercel- TCGATGACCGTTTGGATAAGAGAACTTG-3, DtAux1_GSP2_ lular infection pathway in D. trinervis begins with the invasion of 3 5-GGTCTTGGGATGACCACCTATACGGCTT-3, DtAux1_G the root epidermal and cortical cells by Frankia that penetrates SP1c_3 5- TTTGTGGTAGGGTTTGGGTTCGGTGGAT-3 and theroottissuethroughtheintercellularspacesinbetweenadja- DtAux1_GSP2c_3 5-ATACCGGCACCTCCGCATCACTAGA cent epidermal root cells. Frankia infection triggers cell divisions AAA-3. CDS sequence was amplified by PCR on cDNA extracted in the pericycle leading to the formation of a nodule primordium. from roots using primers DtAux1_cDNA_Fw 5-ATGTTGGC The nodule primordium gives rise to the mature nodule com- TCAGAAACAAGCAG-3, and DtAux1_cDNA_Rv 5-CTAGT prising several lobes. Each lobe is structurally very similar to a GATGCGGAGGTGCC-3.QuantitativePCRwasperformed lateral root with a central vascular bundle, a well-developed cor- on cDNAs extracted from nodules and non-inoculated roots tex and an apical meristem. Neither root hair deformation nor as described (Svistoonoff et al., 2013) using primers DtAux1F infection thread formation takes place as in C. glauca. The pren- 5-ACGGCATGACCACCAAAGG and DtAux1R 5GGTTACTC odule, a small protuberance that originates from cortical cells ACTCTGCTCCATCC-3 to amplify a DtAux1 fragment and divisions beneath of a Frankia infected root hair, is also absent in DtUbiF 5-TACCACCACGAAGACGGAGGAC-3 and DtUbiR the intercellular infection in D. trinervis.IncontrasttoC. glauca, 5-GGAAGCAGTTGGAGGATGGAAGG to amplify an ubiquitin Frankia remains intercellular during the early steps of the infec- fragment used as an internal standard. The sequence of DtAUX1 tion process in D. trinervis and only becomes intracellular once was deposited at Genbank and was given the accession number the bacteria reach the cortical cells of nodule primordia (Valverde KM200713. and Wall, 1999). Very little is known about the mechanisms For the phylogenetic analysis coding sequences of the AUX- involved in intercellular infection in actinorhizal plants. Here, we LAX family of auxin influx carriers were retrieved by family blast analyzed the role of auxin in intercellular infection of D. trinervis search in the Phytozome v9.1 database (www.phytozome.org) by Frankia. using the coding sequence of DtAUX1 as the query. Sequences of AUX-LAX family from D. glomerata were retrieved using MATERIALS
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