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. 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Publications produced within the project:

[1] 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 

[2] 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 

[3] 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 

[4] 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 

[5] 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

[6] 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

[7] 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

[8] 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 

[9] 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

[10] 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 

[11] 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

[12] 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 

[13] 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

[14] 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 

[15] 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 

[16] 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 

[17] 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 

[18]  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

[19] 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. 

[20] 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. 

[21] 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

[22] 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. 

[23] 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

[24] 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/

[25] 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/

[26] 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

[27] 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
https://www.mdpi.com/2218-273X/11/6/898/html

[28] 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

[29] 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

[30] 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

[31] 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 .

[32] 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

[33] 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

[35] 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

[36] 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

[37] 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 .

[38] 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

[39] 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

[40] 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

[41] 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

[42] 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

[43] 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

[44] 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

[45] 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

[46] 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

[47] 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

[48] 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.

[49] 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.

[50] 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

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Contact

Project leaderProject leader

David B. Collinge
dbc@plen.ku.dk
+45 35333356

Funding

The project has received funding from the European Union’s Horizon 2020 research and innovation
programme under the Marie Sklodowska-Curie grant agreement No 676480.

Project: BestPass 
Start:  1. September 2015
End:  30. November 2019