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Monitoring of Rice Transcriptional Responses to Contrasted Colonizing Patterns of Phytobeneficial Burkholderia S.L

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Monitoring of Rice Transcriptional Responses to Contrasted Colonizing Patterns of Phytobeneficial Burkholderia S.L ORIGINAL RESEARCH published: 24 September 2019 doi: 10.3389/fpls.2019.01141 Monitoring of Rice Transcriptional Responses to Contrasted Colonizing Patterns of Phytobeneficial Burkholderia s.l. Reveals a Temporal Shift in JA Systemic Response Eoghan King 1, Adrian Wallner 1, Isabelle Rimbault 1, Célia Barrachina 2, Agnieszka Klonowska 1, Lionel Moulin 1 and Pierre Czernic 1* 1 IRD, CIRAD, University of Montpellier, IPME, Montpellier, France, 2 Montpellier GenomiX (MGX), c/o Institut de Génomique Fonctionnelle, Montpellier, France In the context of plant–pathogen and plant–mutualist interactions, the underlying molecular Edited by: bases associated with host colonization have been extensively studied. However, it is Massimiliano Morelli, Italian National Research Council not the case for non-mutualistic beneficial interactions or associative symbiosis with (IPSP-CNR), Italy plants. Particularly, little is known about the transcriptional regulations associated with the Reviewed by: immune tolerance of plants towards beneficial microbes. In this context, the study of the Stéphane Compant, Burkholderia rice model is very promising to describe the molecular mechanisms involved Austrian Institute of Technology (AIT), Austria in associative symbiosis. Indeed, several species of the Burkholderia sensu lato (s.l.) Lisa Sanchez, genus can colonize rice tissues and have beneficial effects; particularly, two species have Université de Reims Champagne-Ardenne, been thoroughly studied: Burkholderia vietnamiensis and Paraburkholderia kururiensis. France This study aims to compare the interaction of these species with rice and especially to *Correspondence: identify common or specific plant responses. Therefore, we analyzed root colonization Pierre Czernic of the rice cultivar Nipponbare using DsRed-tagged bacterial strains and produced the [email protected] transcriptomes of both roots and leaves 7 days after root inoculation. This led us to the Specialty section: identification of a co-expression jasmonic acid (JA)-related network exhibiting opposite This article was submitted to regulation in response to the two strains in the leaves of inoculated plants. We then Plant Microbe Interactions, a section of the journal monitored by quantitative polymerase chain reaction (qPCR) the expression of JA-related Frontiers in Plant Science genes during time course colonization by each strain. Our results reveal a temporal shift Received: 21 June 2019 in this JA systemic response, which can be related to different colonization strategies of Accepted: 21 August 2019 both strains. Published: 24 September 2019 Citation: Keywords: RNAseq, endophyte, symbiosis, Burkholderia, rice, jasmonic acid King E, Wallner A, Rimbault I, Barrachina C, Klonowska A, Moulin L and Czernic P (2019) Monitoring INTRODUCTION of Rice Transcriptional Responses to Contrasted Colonizing Patterns Plant microbiome is nowadays extensively studied, as it represents a huge potential for agriculture. of Phytobeneficial Burkholderia s.l. Reveals a Temporal Shift in JA Numerous studies describe the importance of microbes for plant’s nutrient supply and resistance to Systemic Response. diseases and pests (Finkel et al., 2017). Therefore, microbes are potential solutions to do the transition Front. Plant Sci. 10:1141. to a sustainable agriculture while maintaining yield (Busby et al., 2017). Especially, some rhizobacteria doi: 10.3389/fpls.2019.01141 have been shown to have tremendous beneficial effects on plant growth (Hayat et al., 2010) Frontiers in Plant Science | www.frontiersin.org 1 September 2019 | Volume 10 | Article 1141 King et al. Rice Sensing of Beneficial Burkholderia and resistance to pathogens (Beneduzi et al., 2012). These and plant-beneficial strains Kaur( et al., 2017). Burkholderia beneficial effects are induced through hormonal modulations vietnamiensis TVV75T (hereafter Bv) is a rice-associated species following the colonization of plant roots (Vacheron et al., 2013) having positive effect on yield Trân( Van et al., 2000; Govindarajan and inner tissues for endophytes (Hardoim et al., 2008) as well et al., 2008), which belongs to the Burkholderia cepacia complex, as systemic regulations of immunity (Pieterse et al., 2014). a complex of species that can cause serious risks to cystic However, the perception of microbe-associated molecular fibrosis patients (Vial et al., 2011). In order to decipher how rice patterns (MAMPs) generally leads to an immune response perceives these two beneficial strains belonging to genera with called MAMPs-triggered immunity (MTI) characterized by contrasted ecologic backgrounds, we studied the transcriptional the synthesis of antimicrobial compounds (Jones and Dangl, responses of rice during the establishment of the interaction. 2006). In the same way pathogens suppress plant immunity, Our aim was to identify plant physiological processes and and beneficial microbes are able to escape Trdá( et al., 2015) or potentially key genes involved in beneficial rice-rhizobacteria modulate (Zamioudis and Pieterse, 2012) the immune response interactions and also differentially regulated by each strain. of plants cells. Interestingly, the suppression of MTI by both We first analyzed the colonization patterns ofPk and Bv on the pathogenic bacteria (Millet et al., 2010) and beneficial fungi Oryza sativa Nipponbare genotype. We then analyzed the root (Jacobs et al., 2011) is commonly mediated via the jasmonic and leaf transcriptional responses to the bacterial colonization acid (JA) signaling pathway. However, the global physiological by RNAseq. This led us to the identification of a co-expression response and especially the transcriptional regulations induced JA-related network. Therefore, we monitored, throughout the by plants during the interaction with beneficial bacteria are not establishment of the interaction, the expression of JA-related well described. genes by reverse transcriptase–quantitative polymerase chain The interaction between plants and rhizospheric or reaction (RT-qPCR). endophytic bacteria-forming associative symbioses has been studied in several species belonging to the genera Azoarcus, Azospirillum, Herbaspirillum, Acetobacter, Gluconacetobacter, MATERIALS AND METHODS Bacillus, Phyllobacterium, Pseudomonas, and (Para-) Plants and Bacterial Cultivation Burkholderia (Ahemad and Kibret, 2014). Most studies on these models focused on the bacterial response to the interaction O. sativa L. ssp. japonica cv Nipponbare was used in this study. with its host plant (Shidore et al., 2012; Coutinho et al., 2015; For all experiments, seeds were dehusked and sterilized as Sheibani-Tezerji et al., 2015), while relatively few studies follows: 70% ethanol for 10 min and 9.6% NaClO supplemented analyzed the transcriptional response of plants. Nonetheless, with 1% Tween 20 for 30 min. Treated seeds were rinsed twice several studies described plants’ transcriptional regulations with sterile distilled water, twice with 2% thiosulfate solution, including lowering of defense (Bordiec et al., 2011; Rekha et al., and finally four times with sterile distilled water. To confirm 2018), hormonal signaling (Drogue et al., 2014; Rekha et al., surface sterilization, 100 µl of the last rinsing solution was 2018), developmental reprogramming (Paungfoo-Lonhienne plated in tryptic soy agar (TSA) medium (Sigma-Aldrich). et al., 2016), and iron homeostasis (Brusamarello-Santos et al., Seeds were then put in sterile distilled water at 28°C for 24 h 2019; Stringlis et al., 2018). and transferred on 8% H2O agar plate for 30 h. Homogeneously Within the diversity of bacteria interacting with plants, the germinated seeds were transferred to sterile magenta boxes Burkholderia sensu lato (s.l.) genus of Betaproteobacteria stands (SPL Lifesciences Co. Ltd) containing 150 ml of autoclaved out for several reasons. It contains plant pathogenic species perlite and 200 ml of sterile hydroponic medium (recipe in (B glumae, Burkholderia gladioli, and Burkholderia plantarii) Supplementary Table 1). Plants were grown in a growth chamber (16 h light; 8 h dark; 28°C; 70% humidity). (Maeda et al., 2006), N2-fixing nodule-forming species in association with tropical legumes (Gyaneshwar et al., 2011) All bacterial strains (listed in Supplementary Table 2) were as well as species-forming associative symbiosis particularly cultured as follows: Glycerol stocks (20%) of bacterial cells with cereals such as rice (Coutinho et al., 2013; Govindarajan conserved at −80°C were plated in low-salt lysogeny broth et al., 2008). Also, a phylogenetic separation discriminates the (LB) (Sigma-Aldrich) agar plates and incubated for 72 h at Burkholderia sensu stricto (s.s.) genus, which contains animal 28°C. Liquid low salt LB medium of 20 ml was then inoculated or plants pathogens as well as human opportunists, and the in 50-ml Falcon tubes and incubated for 16 h under agitation Paraburkholderia genus, which contains mainly plant-associated (180 rpm) at 28°C. Overnight culture of 500 µl was inoculated in and environmental species (Sawana et al., 2014; Estrada-de los fresh liquid medium for 2 h. Bacterial cells were then centrifuged for 5 min at 4,000 rpm and resuspended in sterile distilled water. Santos et al., 2016). Also, most recent phylogenetic refinements 7 of Burkholderia s.l. taxa defined other genera—Caballeronia, Each plantlet was inoculated with 10 bacterial cells 4 days after Robbsia, Trinickia, and Mycetohabitans—which are supported by sowing in hydroponic system. both differences
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