University of Oulu

Koskimäki, J. J., Pohjanen, J., Kvist, J., Fester, T., Härtig, C., Podolich, O., Fluch, S., Edesi, J., Häggman, H., & Pirttilä, A. M. (2022). The meristem-associated endosymbiont Methylorubrum extorquens DSM13060 reprograms development and stress responses of pine seedlings. Tree Physiology, 42(2), 391–410.

The meristem-associated endosymbiont Methylorubrum extorquens DSM13060 reprograms development and stress responses of pine seedlings

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Author: Koskimäki, Janne J.1; Pohjanen, Johanna1; Kvist, Jouni2;
Organizations: 1Ecology and Genetics Research Unit, University of Oulu, Paavo Havaksentie J1, FI-90014 Oulu, Finland
2Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Haartmaninkatu 8, FI-00014 Helsinki, Finland
3Department of Environmental Microbiology, Helmholtz Centre for Environmental Research – UFZ, Permoserstr. 15, 04318 Leipzig, Germany
4Institute of Molecular Biology and Genetics of NASU, Acad. Zabolotnoho str., 150 03680 Kyiv, Ukraine
5Weiden am See, Burgenland 7121, Austria
6Production Systems, Tree Breeding, Natural Resources Institute Finland LUKE, FI-57200 Savonlinna, Finland
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 2.1 MB)
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Language: English
Published: Oxford University Press, 2022
Publish Date: 2022-03-14


Microbes living in plant tissues—endophytes—are mainly studied in crop plants where they typically colonize the root apoplast. Trees—a large carbon source with a high capacity for photosynthesis—provide a variety of niches for endophytic colonization. We have earlier identified a new type of plant–endophyte interaction in buds of adult Scots pine, where Methylorubrum species live inside the meristematic cells. The endosymbiont Methylorubrum extorquens DSM13060 significantly increases needle and root growth of pine seedlings without producing plant hormones, but by aggregating around host nuclei. Here, we studied gene expression and metabolites of the pine host induced by M. extorquens DSM13060 infection. Malic acid was produced by pine to potentially boost M. extorquens colonization and interaction. Based on gene expression, the endosymbiont activated the auxin- and ethylene (ET)-associated hormonal pathways through induction of CUL1 and HYL1, and suppressed salicylic and abscisic acid signaling of pine. Infection by the endosymbiont had an effect on pine meristem and leaf development through activation of GLP1–7 and ALE2, and suppressed flowering, root hair and lateral root formation by downregulation of AGL8, plantacyanin, GASA7, COW1 and RALFL34. Despite of systemic infection of pine seedlings by the endosymbiont, the pine genes CUL1, ETR2, ERF3, HYL, GLP1–7 and CYP71 were highly expressed in the shoot apical meristem, rarely in needles and not in stem or root tissues. Low expression of MERI5, CLH2, EULS3 and high quantities of ononitol suggest that endosymbiont promotes viability and protects pine seedlings against abiotic stress. Our results indicate that the endosymbiont positively affects host development and stress tolerance through mechanisms previously unknown for endophytic bacteria, manipulation of plant hormone signaling pathways, downregulation of senescence and cell death-associated genes and induction of ononitol biosynthesis.

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Series: Tree physiology
ISSN: 0829-318X
ISSN-E: 1758-4469
ISSN-L: 0829-318X
Volume: 42
Issue: 2
Pages: 391 - 410
DOI: 10.1093/treephys/tpab102
Type of Publication: A1 Journal article – refereed
Field of Science: 1183 Plant biology, microbiology, virology
Funding: This work was funded by the Academy of Finland (project no. 308766).
Academy of Finland Grant Number: 308766
Detailed Information: 308766 (Academy of Finland Funding decision)
Dataset Reference: The gene expression data has been submitted to Genbank’s GEO ( under the accession no. GSE170995.
Copyright information: © The Author(s) 2021. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.