BestPass - Boosting Plant-Endophyte Stability, Compatibility and Performance across scales
PROJECT IS COMPLETED
Project period: 2015 to 2019
BestPass project was an Innovative Training Network (ITN) funded by the European Union’s Horizon 2020 research and innovation programme. The project focused producing knowledge about the use of endophytes to improve plant productivity in a sustainable way.
Plant endophytic microorganisms can improve plant yield and enhance plant tolerance to abiotic stress as well as to pathogens under experimental conditions, but these effects are often not sufficiently stable for practical application. BestPass addressed these concerns and successfully trained a new generation of bright researchers who gained a profound understanding of the potential for endophytes in contributing to the next green revolution.
BestPass provided a unique opportunity for 15 Early Stage researchers (ESRs) to obtain the knowledge and skills needed to develop and utilize new technologies for understanding and using endophytes to improve plant productivity in a sustainability way.
Societal challenges addressed in BestPass
Global food production is facing a number of major challenges over the coming century. The global population is growing and becoming increasingly urban and sophisticated in their diet. The climate is changing and becoming more unpredictable. To meet these and other challenges we need to increase crop yields while reducing pesticide input and use of inorganic fertiliser. Plant endophytic microorganisms can contribute to these goals by improving plant yield and enhancing plant tolerance to abiotic stress as well as to pathogens under experimental conditions, but these effects are often not sufficiently stable for practical application.
The effects of endophytes on plants
We need to understand the genetic basis of beneficial interactions between crops and endophytes and extend this basic knowledge of phenotypic plasticity to all interaction levels from the cellular to the field environment. This requires research into the molecular mechanisms underlying the effects of endophytes, including intra and inter-kingdom exchange and distribution of resources (nutrients). The genetic variation and its plasticity in host and microbe will be exploited in order to establish crop breeding and inoculum production processes for boosting the establishment and stability of plant-microbe mutualisms to benefit crop development, stress tolerance, pathogen resistance and quality.
Overall objectives of BestPass:
- To understand the genetic and mechanistic basis of plant – endophyte interactions.
- To assess these interactions for improving plant yield and quality under abiotic and biotic stress conditions.
- To boost the stability and reliability of the beneficial effects of endophytes or endophyte consortia on plants.
- To provide the best possible training to support the career development of the Early Stage Researchers (ESRs) in the field of beneficial plant microbe interactions.
The BestPass project consisted of major research groups from leading universities, research institutes and key biotechnology companies. The highly innovative and multidisciplinary consortium entailed 6 European countries and New Zealand. BestPass was coordinated by the University of Copenhagen and consisted of the following 12 beneficiaries:
Leibniz-Institut für Gemüse- und Zierpflanzenbau Grossbeeren/Erfurt E.V.
Agencia Estatal Consejo Superior de Investigaciones Cientificas
Nicolaus Copernicus University (UNIWERSYTET MIKOLAJA KOPERNIKA W TORUNIU)
Austrian Institute of Technology GmbH
The BestPass project has made stable progress in its activities with contributions from the entire consortium throughout the project period. The main results achieved in the project includes:
- Phytohormones impact on fungal endophyte communities in tomato roots.
- Changes in plant hormone levels upon colonization of tomato by endophytic and/or pathogenic strains of F. oxysporum.
- Identification of P-solubilising bacteria and interaction with an AM fungus.
- Characterization of grass populations with improved endophyte compatibility.
- Detection and characterization of genotypic variation in Epichloë spp. using microsatellite markers.
Approximately half of the papers expected from the project have been published (23 publications) at the time of project closure, therefore more publishable and disseminated results are still expected. Furthermore, one patent has been filled as an output from BestPass, as a joint invention between the Universities of Copenhagen and Michigan State.
The project has provided excellent training for the ESRs in the areas of genomics, bioinformatics, plant physiology, industrial production of microbial inoculants/products and endophyte performance.
Little was known in advance of the study about the microbes or molecules involved in the biological interactions under study. But BestPass has yielded new knowledge, which is exploitable and/or publishable, and has provided materials and techniques for improving crop plant productivity. BestPass has, moreover, formed a new generation of scientists with deep knowledge in basic research, and who possess the awareness of the challenge to bring this knowledge to practical applications.
Management of BestPass in the University of Copenhagen:
David B. Collinge - project coordinator
Phone: +45 35333356
Minttu Liuhto - project manager
Phone: +45 35334006
Publications produced within the project:
 Bedini, A., Mercy, L., Schneider, C., Franken, P. and Lucic-Mercy, E. (2018) Unraveling the Initial Plant Hormone Signaling, Metabolic Mechanisms and Plant Defense Triggering the Endomycorrhizal Symbiosis Behavior, Frontiers in Plant Science, 9, doi:10.3389/fpls.2018.01800
 Di, X., Cao, L., Hughes, R. K., Tintor N., Banfield, M J. and Takken F. L. W. (2017) Structure-function analysis of the Fusarium oxysporum Avr2 effector allows uncoupling of its immune-suppressing activity from recognition, New Phytologist, 216/3, doi:10.1111/nph.14733
 Di, X., Takken, F. L. W. and Tintor, N. (2016) How Phytohormones Shape Interactions between Plants and the Soil-Borne Fungus Fusarium oxysporum, Fron. in Plant Science, 7, doi:10.3389/fpls.2016.00170
 Mülner, P., Bergna, A., Wagner, P., Sarajlic, D., Gstöttenmay, B., Dietel, K., Grosch, R., Cernava, T. and Berg, G. (2019) Microbiota Associated with Sclerotia of Soilborne Fungal Pathogens – A Novel Source of Biocontrol Agents Producing Bioactive Volatiles, Phytobiomes Journal, 3/2, doi:10.1094/pbiomes-11-18-0051-r
 Bergna, A., Cernava, T., Rändler, M., Grosch, R., Zachow, C. and Berg, G. (2018) Tomato Seeds Preferably Transmit Plant Beneficial Endophytes, Phytobiomes Journal, 2/4, doi:10.1094/pbiomes-06-18-0029-r
 Franken, P., Takken, F. L. W. and rep, M. (2019) Transcript accumulation in a trifold interaction gives insight into mechanisms of biocontrol, New Phytologist, 224/2, doi:10.1111/nph.16141
 Furtado, B. U., Gołębiewski, M., Skorupa M., Hulisz, P., and Hrynkiewicz, K. (2019) Bacterial and Fungal Endophytic Microbiomes of Salicornia europaea, Applied and Env. Microbiology, 85/13, doi: 10.1128/aem.00305-19
 Furtado, B. U., Nagy, I., Asp, T., Jarosław Tyburski, J., Skorupa, M., Gołębiewski, M., Hulisz, P., and Hrynkiewicz, K. (2019) Transcriptome profiling and environmental linkage to salinity across Salicornia europaea vegetation, BMC Plant Biology, 19/1, doi:10.1186/s12870-019-2032-3
 Pereira, E., Vázquez de Aldana, B. R., San Emeterio, L, and Zabalgogeazcoa, I. (2019) A Survey of Culturable Fungal Endophytes From Festuca rubra subsp. pruinosa, a Grass From Marine Cliffs, Reveals a Core Microbiome, Front. in Microbiology, 9, doi:10.3389/fmicb.2018.03321
 Cagnano, G., Roulund, N., Jensen, C. S., Forte F., Asp, T., and Leuchtmann, A. (2019) Large Scale Screening of Epichloë Endophytes Infecting Schedonorus pratensis and Other Forage Grasses Reveals a Relation Between Microsatellite-Based Haplotypes and Loline Alkaloid Levels, Front. in Plant Science, 10, doi:10.3389/fpls.2019.00765
 Collinge, D. B., Jørgensen, H. J. L., Latz, M., Manzotti, A., Ntana, F., Rojas, E., and Jensen, B. (2019) Searching for Novel Fungal Biological Control Agents for Plant Disease Control Among Endophytes, 25-51, doi:10.1017/9781108607667.003
 Furtado, B. U., Szymańska, S., and Hrynkiewicz, K. (2019) A window into fungal endophytism in Salicornia europaea: deciphering fungal characteristics as plant growth promoting agents, Plant and Soil, 445/1-2, doi:10.1007/s11104-019-04315-3
 Di, X., Gomila, J., Ma, L., van den Burg, H. A., and Takken, F. L. W. (2016) Uptake of the Fusarium Effector Avr2 by Tomato Is Not a Cell Autonomous Event, Front. in Plant Science, 7, doi: 10.3389/fpls.2016.01915
 Di, X., Gomila, J. and Takken, F. L. W. (2017) Involvement of salicylic acid, ethylene and jasmonic acid signalling pathways in the susceptibility of tomato to Fusarium oxysporum, Molecular Plant Pathology, 18/7, doi: 10.1111/mpp.12559
 Cao, L., Blekemolen, M. C., Tintor, N., Cornelissen, B., and Takken, F. L. W. (2018) The Fusarium oxysporum Avr2-Six5 Effector Pair Alters Plasmodesmatal Exclusion Selectivity to Facilitate Cell-to-Cell Movement of Avr2, Molecular Plant, 11/5, doi: 10.1016/j.molp.2018.02.011
 Acevedo-Garcia, J., Gruner, K., Reinstädler, A., Kemen, A., Kemen, E., Cao, L., Takken, F. L. W., Reitz, M., Schäfer, P., O’Connell, R., Kusch, S., Kuhn, H., and Panstruga, R. (2017) The powdery mildew-resistant Arabidopsis mlo2 mlo6 mlo12 triple mutant displays altered infection phenotypes with diverse types of phytopathogens, Scientific Reports, 7/1, doi: 10.1038/s41598-017-07188-7
 Wróblewski, T., Spiridon, L., Martin, E. C., Petrescu, A-J., Cavanaugh, K., Truco, M. J., Xu, H., Gozdowski, D., Pawłowski, K., Michelmore, R. W., and Takken, F. L. W. (2018) Genome-wide functional analyses of plant coiled–coil NLR-type pathogen receptors reveal essential roles of their N-terminal domain in oligomerization, networking, and immunity, PLOS Biology, 16/12, doi 10.1371/journal.pbio.2005821
 de Lamo, F., Constantin, M. E., Fresno, D. H., Boeren, S., Rep, M., and Takken, F. L. W. (2018) Xylem Sap Proteomics Reveals Distinct Differences Between R Gene- and Endophyte-Mediated Resistance Against Fusarium Wilt Disease in Tomato,Frontiers in Microbiology 9, doi 10.3389/fmicb.2018.02977
 Tintor, N., Paauw, M., Rep, M., and Takken F. L. W. (2020) The root-invading pathogen Fusarium oxysporum targets pattern-triggered immunity using both cytoplasmic and apoplastic effectors, New Phytol. doi: 10.1111/nph.16618.
 Constantin, M. E., Vlieger B. V., Takken, F. L. W., and Rep, M (2020) Diminished Pathogen and Enhanced Endophyte Colonization upon CoInoculation of Endophytic and Pathogenic Fusarium Strains. Microorganisms, 8(4):544. doi: 10.3390/microorganisms8040544.
 De Lamo, F. J. and Takken, F. L. W. (2020) Biocontrol by Fusarium oxysporum Using Endophyte-Mediated Resistance. Front Plant Sci. 11: 37 2020. doi: 10.3389/fpls.2020.00037.
 Constantin M. E., de Lamo, F. J., Vlieger, B. V., rep, M. and Takken F. L. W. (2019) Endophyte-Mediated Resistance in Tomato to Fusarium oxysporum Is Independent of ET, JA, and SA. Front Plant Sci. 10:979. eCollection 2019. doi: 10.3389/fpls.2019.00979.
 Manzotti, A., Bergna, A., Burow, M., Jørgensen, H. J. L., Cernava, T., Berg, G., Collinge, D. B. and Jensen, B. (2020) Insight into the community structure and lifestyle of the fungal root endophytes of tomato by combining amplicon sequencing and isolation approaches with phytohormone profiling. FEMS Microbiology Ecology, 96:5, https://doi.org/10.1093/femsec/fiaa052.
 De Lamo, F. J., Spijkers, S. B. and Takken, F. L. W. (2020) Protection to tomato wilt disease conferred by the non-pathogen Fusarium oxysporum Fo47 is more effective than that conferred by avirulent strains. Phytopathology 111: 253-257, https://pubmed.ncbi.nlm.nih.gov/32720878/
 Richard, M. M. S., Knip, M., Aalders, T. et al. (2020) Unlike many disease resistances , Rxl-Meditated immunity to potato virus X is not compromised at elevated temperatures. Frontiers in Genetics, 11:417, https://pubmed.ncbi.nlm.nih.gov/32391063/
 Forte FP, Schmid J, Dijkwel PP, et al., 2020. Fungal Endophyte Colonization Patterns Alter Over Time in the Novel Association Between Lolium perenne and Epichloë Endophyte AR37. Frontiers in Plant Science 11. https://www.frontiersin.org/articles/10.3389/fpls.2020.570026/full
 Ntana F, Bhat WW, Johnson SR, Jørgensen HJL, Collinge DB, Jensen B and Hamberger B. (2021) A sesquiterpene synthase from the endophytic fungus Serendipita indica catalyses formation of viridiflorol. Biomolecules 11: 898. doi:10.3390/biom11060898
 Pereira EC, Vazquez de Aldana BR, Arellano JB, Zabalgogeazcoa I. 2021 The role of fungal microbiome components on the adaptation to salinity of Festuca rubra subsp. pruinosa. Frontiers in Plant Science 12: 695717. https://doi.org/10.3389/fpls.2021.695717
 Ntana F, Johnson SR, Hamberger B, Jensen B, Jørgensen HJL, Collinge DB. 2022 Regulation of Tomato Specialised Metabolism after Establishment of Symbiosis with the Endophytic Fungus Serendipita indica. Microorganisms 10: 194. https://doi.org/10.3390/microorganisms10010194
 Del Barrio-Duque A, Ley J, Samad A, Antonielli L, Sessitsch A, Compant S, 2019. Beneficial Endophytic Bacteria-Serendipita indica Interaction for Crop Enhancement and Resistance to Phytopathogens. Frontiers in Microbiology 10. https://doi.org/10.3389/fmicb.2019.02888
 Constantin ME, De Lamo FJ, Rep M, Takken FLW, 2020. From laboratory to field: applying the Fo47 biocontrol strain in potato fields. European Journal of Plant Pathology 158: 645-54. http://dx.doi.org/10.1007/s10658-020-02106-6 .
 Richard MMS, Knip M, Aalders T, Beijaert MS, Takken FLW, 2020. Unlike many disease resistances, Rx1-mediated immunity to Potato Virus X Is not compromised at elevated temperatures. Frontiers in Genetics 11. http://dx.doi.org/10.3389/fgene.2020.00417
 Del Barrio-Duque A, Samad A, Nybroe O, Antonielli L, Sessitsch A, Compant S, 2020. Interaction between endophytic Proteobacteria strains and Serendipita indica enhances biocontrol activity against fungal pathogens. Plant and Soil 451: 277-305. https://link.springer.com/article/10.1007%2Fs11104-020-04512-5
 Sharma S, Compant S, Ballhausen M-B, Ruppel S, Franken P, 2020. The interaction between Rhizoglomus irregulare and hyphae attached phosphate solubilizing bacteria increases plant biomass of Solanum lycopersicum. Microbiological Research 240, 126556. https://doi.org/10.1016/j.micres.2020.126556
 De Lamo FJ, Šimkovicová M, Fresno DH, et al., 2021. Pattern-triggered immunity restricts host colonization by endophytic Fusaria, but does not affect endophyte-mediated resistance. Molecular Plant Pathology 22, 204-15. http://dx.doi.org/10.1111/mpp.13018
 Richard MMS, Knip M, Schachtschabel J, Beijaert MS, Takken FLW, 2021. Perturbation of nuclear–cytosolic shuttling of Rx1 compromises extreme resistance and translational arrest of potato virus X transcripts. The Plant Journal 106, 468-79. http://dx.doi.org/10.1111/tpj.15179 .
 Constantin ME, Fokkens L, De Sain M, Takken FLW, Rep M, 2021. Number of candidate effector genes in accessory genomes differentiates pathogenic from endophytic Fusarium oxysporum strains. Frontiers in Plant Science 12. https://doi.org/10.3389/fpls.2021.761740
 Sharma S, Compant S, Franken P, Ruppel S, Ballhausen M-B, 2021. It takes two to tango: A bacterial biofilm provides protection against a fungus-feeding bacterial predator. Microorganisms 9: 1566. https://doi.org/10.3390/microorganisms9081566
 Cagnano G, Roulund N, Jensen CS, Lenk I, Cox MP and Asp T. 2020. Mycelial biomass and concentration of loline alkaloids driven by complex population structure in Epichloë uncinata and meadow fescue (Schedonorus pratensis). Mycologia, 112(3): 474–490. https://doi.org/10.1080/00275514.2020.1746607
 Cagnano G, Vázquez-de-Aldana BR, Asp T, Roulund N, Jensen CS, Soto-Barajas MC. 2020 Determination of loline alkaloids and mycelial biomass in endophyte infected Schedonorus pratensis by near-infrared spectroscopy and chemometrics. Microorganisms, 8:776. https://doi.org/10.3390/microorganisms8050776 https://www.mdpi.com/2076-2607/8/5/776
 Furtado BU, Hrynkiewicz K. Halophyte–Endophyte Interactions: Linking microbiome community distribution and functionality to salinity. InSymbiotic Soil Microorganisms 2021, Springer, Cham (pp. 363-377) https://doi.org/10.1007/978-3-030-51916-2_21
 Rändler-Kleine M., Wolfgang A., Dietel K., Junge H., Cernava T., Berg G. (2020) How Microbiome Approaches Can Assist Industrial Development of Biological Control Products. In: Gao Y., Hokkanen H., Menzler-Hokkanen I. (eds) Integrative Biological Control. Progress in Biological Control, vol 20. Springer, Cham. https://doi.org/10.1007/978-3-030-44838-7_13
 Mülner, P., Schwarz, E., Dietel, K., Junge, H., Herfort, S., Weydmann, M., Lasch, P., Cernava, T., Berg, G. & Vater, J. (2020). Profiling for bioactive peptides and volatiles of plant growth promoting strains of the bacillus subtilis complex of industrial relevance. Frontiers in Microbiology, 11, 1432. Doi: https://doi.org/10.3389/fmicb.2020.01432
 Mülner, P., Schwarz, E., Dietel, K., Herfort, S., Jähne, J., Lasch, P., Cernava, T., Berg, G. & Vater, J. (2021). Fusaricidins, Polymyxins and Volatiles Produced by Paenibacillus polymyxa Strains DSM 32871 and M1. Pathogens, 10, 1485. Doi: https://doi.org/10.3390/pathogens10111485
 Kusstatscher P, Wicaksono WA, Bergna A, et al., 2020. Trichomes form genotype-specific microbial hotspots in the phyllosphere of tomato. Environmental Microbiome 15, 17. https://doi.org/10.1186/s40793-020-00364-9
 Sarrocco S, Herrera-Estrella A, Collinge DB, 2020. Editorial: Plant Disease Management in the Post-genomic Era: From Functional Genomics to Genome Editing. Frontiers in Microbiology 11. DOI https://doi.org/10.3389/fmicb.2020.00107
 Taffner J, Bergna A, Cernava T, Berg G, 2020. Tomato-Associated Archaea Show a Cultivar-Specific Rhizosphere Effect but an Unspecific Transmission by Seeds. Phytobiomes Journal 4, 133-41.
 De Lamo FJ, Šimkovicová M, Fresno DH, et al., 2021. Pattern-triggered immunity restricts host colonization by endophytic fusaria, but does not affect endophyte-mediated resistance. Molecular Plant Pathology 22, 204-15.
 De Rocchis V, Roitsch T, Franken P, 2022. Extracellular Glycolytic Activities in Root Endophytic Serendipitaceae and Their Regulation by Plant Sugars. Microorganisms 10, 320. https://doi.org/10.3390/microorganisms10020320
 Pereira EC, Zabalgogeazcoa I, Arellano JB, Ugalde U and Vázquez de Aldana BR (2023) Diaporthe atlantica enhances tomato drought tolerance by improving photosynthesis, nutrient uptake and enzymatic antioxidant response. Front. Plant Sci. 14:1118698. doi: https://doi.org/10.3389/fpls.2023.1118698
 Collinge DB, Jensen B, Jørgensen HJL (2022) Fungal Endophytes in Plants and their Relationship to Plant Disease. Current Opinion in Microbiology 69: 102177 https://doi.org/10.1016/j.mib.2022.102177
BestPass recruited the following 15 PhD students:
- ESR1 - Bliss Ursula Furtado
Nicolaus Copernicus University, Torun, Poland
- ESR2 - Eric Carvalho Pereira
University of Salamanca, Spain
- ESR3 - Flavia Pilar Forte
Aarhus University, Denmark
- ESR4 - Alessandro Bergna
ACIB GmbH - TU Graz, Austria
- ESR5 - Andrea Manzotti
University of Copenhagen, Denmark
- ESR6 - Francisco J. de Lamo
University of Amsterdam, Netherlands
- ESR7 - Maria E. Constantin
University of Amsterdam, Netherlands
- ESR8 - Fani Ntana
University of Copenhagen, Denmark
- ESR9 - Vincenzo De Rocchis
Humboldt University, Germany / University of Copenhagen, Denmark
- ESR10 - Alejandro del Barrio
Austrian Institute of Technology (AIT), Austria
- ESR11 - Giovanni Cagnano
- ESR12 - Pascal Muelner
ABiTEP GmbH, Germany
- ESR13 - Manuela Randler- Kleine
Technical University of Graz, Austria
- ESR14 - Shubhangi Sharma
Humbolt University, Germany
- ESR15- Alberico Bedini
INOQ GmbH, Germany
David B. Collinge