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Differences in Resources Use Lead to Coexistence of Seed-Transmitted Microbial

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bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Title page 2 Title: Differences in resources use lead to coexistence of seed-transmitted microbial 3 populations 4 Autors and affiliations : Torres-Cortés G1, Garcia BJ2, Compant S3, Rezki S1, Jones P2, 5 Préveaux A1, Briand M1, Roulet A4, Bouchez O4, Jacobson D2, Barret M1* 6 7 1IRHS, Agrocampus-Ouest, INRA, Université d’Angers, SFR4207 QuaSaV, 49071 8 Beaucouzé, France. 9 2Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA 10 3AIT Austrian Institute of Technology GmbH, Center for Health and Bioresources, 11 Bioresources Unit, Konrad Lorenz Straße 24, A-3430 Tulln, Austria. 12 4INRA, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France. 13 14 Authors email addresses: 15 Gloria Torres-Cortés: [email protected] 16 Benjamin James Garcia: [email protected] 17 Stéphane Compant: [email protected] 18 Samir Rezki: [email protected] 19 Piet Jones: [email protected] 20 Anne Préveaux: [email protected] 21 Martial Briand: [email protected] 22 Alain Roulet: [email protected] 23 Olivier Bouchez: [email protected] 24 Daniel Jacobson: [email protected] 25 Matthieu Barret: [email protected] 26 27 *Corresponding author 1 bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 28 IRHS, 42 rue Georges Morel, 49071 Beaucouzé Cedex, France 29 Phone: +33 (0)2 41 22 57 29 30 Fax: +33 (0)2 41 22 57 05 2 bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 31 ABSTRACT 32 Seeds are involved in the vertical transmission of microorganisms in plants and act as 33 reservoirs for the plant microbiome. They could serve as carriers of pathogens, making the 34 study of microbial interactions on seeds important in the emergence of plant diseases. We 35 studied the influence of biological disturbances caused by seed transmission of two 36 phytopathogenic agents, Alternaria brassicicola Abra43 (Abra43) and Xanthomonas 37 campestris pv. campestris 8004 (Xcc8004), on the structure and function of radish seed 38 microbial assemblages, as well as the nutritional overlap between Xcc8004 and the seed 39 microbiome, to find seed microbial residents capable of outcompeting this pathogen. 40 According to taxonomic and functional inference performed on metagenomics reads, no shift 41 in structure and function of the seed microbiome was observed following Abra43 and 42 Xcc8004 transmission. This lack of impact derives from a limited overlap in nutritional 43 resources between Xcc8004 and the major bacterial populations of radish seeds. However, 44 two native seed-associated bacterial strains belonging to Stenotrophomonas rhizophila 45 displayed a high overlap with Xcc8004 regarding the use of resources; they might therefore 46 limit its transmission. The strategy we used may serve as a foundation for the selection of 47 seed indigenous bacterial strains that could limit seed transmission of pathogens. 3 bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 48 INTRODUCTION 49 Plant-associated microbial assemblages (a.k.a plant microbiome) can impact plant 50 fitness through the modification of a number of traits including biomass production, flowering 51 time or resistance to abiotic and biotic stresses1–4. Due to these important effects on plant 52 growth and health, numerous studies have focused mainly on the microbial communities 53 horizontally acquired from the environment and associated with the rhizosphere and 54 phyllosphere5–7. Although the relative contribution of vertical transmission in the ultimate 55 composition of the plant microbiome is probably limited8, vertically-transmitted 56 microorganisms can also have an important impact on plant fitness9. For instance, vertically- 57 transmitted microorganisms can promote germination of seeds through the production of 58 cytokinins10,11 or increase nutrient availability in shoots and roots12. A well-documented 59 example of vertical transmission is seed transmission of plant pathogenic agents. Seed 60 transmission of plant pathogens, including viruses, bacteria and fungi, was initially identified 61 in the late 1800s - early 1900s13. Seed-transmission of plant pathogenic agents serves as a 62 major means of dispersal and can therefore be responsible for disease emergence and 63 spread13,14. Very low degrees of seed contamination by bacterial pathogens can lead to 64 efficient plant colonization15. Furthermore, seed transmission of plant pathogens is usually 65 asymptomatic and can take place on non-host plants16,17, which can then serve as a reservoir 66 of plant pathogens. 67 To control seed transmission of plant pathogens one should either eradicate them 68 on seed-producing crops or perform seed treatments. Fungicide application during plant 69 production or as seed treatment is an effective means of fungal pathogen management18. 70 Since these chemical-base methods are unsatisfactory for bacterial plant pathogens and 71 have a potentially harmful environmental impact19, alternative control methods have been 72 proposed, including seed health testing, physical seed treatment (e.g thermotherapy) and 73 biological methods such as seed coating of specific biocontrol agents14,18. Direct 74 incorporation of biocontrol agents within the seed tissues through inoculation of seed- 4 bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 75 producing crops is of interest to restrict seed transmission of plant pathogenic agents. 76 Recently, this approach (called EndoSeedTM) has been successfully performed by 77 introducing the plant-growth promoting strain Paraburkholderia phytofirmans PsJN into seeds 78 of multiple plant species through spray-inoculation of the parent plant at the flowering 79 stage20. Therefore, inoculation of strain(s) that can compete with plant pathogens for 80 resources and space may be of interest to limit seed transmission of phytopathogenic 81 agents21. 82 Although inoculation of biocontrol microorganisms on or within the seeds may 83 improve seedling health by protecting them against seed-borne or soil-borne pathogens, 84 adequate formulation of these microorganisms for a successful seed colonization and 85 subsequent persistence on seedlings is still challenging18. Further knowledge about the 86 interactions between phytopathogenic agents and other members of the plant microbiome 87 could provide clues on the selection of candidate strains that compete with the target plant 88 pathogen. These microbial interactions can be estimated by analyzing the response of the 89 seed microbiome following seed-transmission of plant pathogens. Indeed, this approach can 90 potentially reveal co-occurence and more importantly exclusion between plant pathogens 91 and resident members of the seed microbiota22. Recently, we initiated such an approach by 92 studying the response of the radish seed microbiome to seed-transmission of two plant 93 pathogens of brassicas, the bacterial strain Xanthomonas campestris pv. campestris 8004 94 (Xcc800423) and the fungal strain Alternaria brassicicola Abra43 (Abra4324,25). These plant 95 pathogens are frequent seed colonizers of a range of Brassicaceae species including 96 cabbage, cauliflower, turnip and radish26,27. Additionally, they differ in their seed transmission 97 pathways: Xcc8004 being seed-transmitted through the systemic and floral pathways while 98 Abra43 being transmitted through the external pathway28–30. 99 According to community profiling approaches, seed transmission of Abra43 100 impacted the taxonomic composition of the fungal fraction of the seed microbiome, while 101 Xcc8004 did not change the structure of the seed microbiota24. The absence of changes in 5 bioRxiv preprint doi: https://doi.org/10.1101/560367; this version posted February 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 102 community structure following Xcc8004 seed transmission could be explained by differences 103 in ecological niches between the plant pathogen and the members
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