Abstract
During arbuscular mycorrhizal symbiosis, colonization of the root is modulated in response to the physiological status of the plant, with regulation occurring locally and systemically. Here, we identify differentially expressed genes encoding CLAVATA3/ESR-related (CLE) peptides that negatively regulate colonization levels by modulating root strigolactone content. CLE function requires a receptor-like kinase, SUNN; thus, a CLE–SUNN–strigolactone feedback loop is one avenue through which the plant modulates colonization levels.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author on request. RNA sequencing raw reads are deposited in the NCBI Sequence Read Archive database (accession number SRP198429).
References
Kobae, Y. et al. Plant Cell Physiol. 59, 544–553 (2018).
Akiyama, K., Matsuzaki, K.-I. & Hayashi, H. Nature 435, 824–827 (2005).
Besserer, A. et al. PLoS Biol. 4, e226 (2006).
Genre, A. et al. New Phytol. 198, 190–202 (2013).
Oldroyd, G. E. D. Nat. Rev. Microbiol. 11, 252–263 (2013).
Menge, J. A. et al. New Phytol. 80, 575–578 (1978).
Breuillin, F. et al. Plant J. 64, 1002–1017 (2010).
Liu, W. et al. Plant Cell 23, 3853–3865 (2011).
Kretzschmar, T. et al. Nature 483, 341–344 (2012).
Vierheilig, H. et al. Soil Biol. Biochem. 32, 589–595 (2000).
Vierheilig, H. J. Plant Physiol. 161, 339–341 (2004).
Meixner, C. et al. Planta 222, 709–715 (2005).
Solaiman, M. Z. et al. J. Plant Res. 113, 443–448 (2000).
Morandi, D. et al. Mycorrhiza 10, 37–42 (2000).
Wang, C., Reid, J. B. & Foo, E. Front. Plant Sci. 9, 988 (2018).
Tsikou, D. et al. Science 362, 233–236 (2018).
Sasaki, T. et al. Nat. Commun. 5, 4983 (2014).
Fletcher, J. C. et al. Science 283, 1911–1914 (1999).
Hastwell, A. H. et al. Sci. Rep. 7, 9384 (2017).
Goad, D. M., Zhu, C. & Kellogg, E. A. New Phytol. 216, 605–616 (2016).
Hirakawa, Y. & Sawa, S. Curr. Opin. Plant Biol. 51, 81–87 (2019).
Funayama-Noguchi, S. et al. J. Plant Res. 124, 155–163 (2011).
Handa, Y. et al. Plant Cell Physiol. 56, 1490–1511 (2015).
Le Marquer, M., Bécard, G. & Frei dit Frey, N. New Phytol. 222, 1030–1042 (2019).
Javot, H. et al. Proc. Natl Acad. Sci. USA 104, 1720–1725 (2007).
Mortier, V. et al. Plant Physiol. 153, 222–237 (2010).
Liao, P. et al. Biotechnol. Adv. 34, 697–713 (2016).
van Zeijl, A. et al. BMC Plant Biol. 15, 260 (2015).
Seto, Y. & Yamaguchi, S. Curr. Opin. Plant Biol. 21, 1–6 (2014).
Gomez-Roldan, V. et al. Nature 455, 189–194 (2008).
Tokunaga, T., Hayashi, H. & Akiyama, K. Phytochemistry 111, 91–97 (2015).
Thuring, J. W. J. F., Nefkens, G. H. L. & Zwanenburg, B. J. Agric. Food Chem. 45, 2278–2283 (1997).
Scaffidi, A. et al. Plant Physiol. 165, 1221–1232 (2014).
Nimchuk, Z. L. et al. Development 142, 1043–1049 (2015).
Schnabel, E. et al. Plant Mol. Biol. 58, 809–822 (2005).
Foo, E., Ferguson, B. J. & Reid, J. B. Ann. Bot. 113, 1037–1045 (2014).
Morandi, D. et al. Mycorrhiza 19, 435–441 (2009).
López-Ráez, J. A. et al. J. Plant Physiol. 168, 294–297 (2011).
Somssich, M. et al. Development 143, 3238–3248 (2016).
Wang, G., Zhang, G. & Wu, M. Front Plant Sci. 6, 1211 (2015).
Acknowledgements
We apologize to those authors whose work we have not cited due to reference number constraints. We thank S. Roh and S. Cotraccia for technical assistance, K. Akiyama (Osaka Prefecture University, Osaka, Japan) for providing an authentic standard of medicaol and B. Zwanenburg (University of Nijmegen, Nijmegen, the Netherlands) for providing rac-GR24. Financial support for the project was provided by the US National Science Foundation grants IOS-1127155 and the US Department of Energy Office of Science, Office of Biological and Environmental Research (grant no. DE-SC0012460). L.M.M. was supported by postdoctoral fellowships from the Swiss National Science Foundation (Early Postdoc.Mobility) and the German Research Foundation (DFG). H.J.B. was supported by the European Research Council (ERC Advanced grant CHEMCOMRHIZO, 670211) and K.F. by the Netherlands Organisation for Scientific Research (NWO-ECHO grant 711.018.010).
Author information
Authors and Affiliations
Contributions
L.M.M. and M.J.H. conceived the experiments and analysed the data. E.S. and J.F. provided genome-level identification of CLE genes and sunn mutants. K.F. and H.J.B. analysed and interpreted strigolactone levels. X.S. and Z.F. processed the RNA sequencing data and generated differential expression data. L.M.M. carried out all other experiments. L.M.M. and M.J.H. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information: Nature Plants thanks Caroline Gutjahr and other, anonymous, reviewers for their contribution to the peer review of this work.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Figs. 1–14, Supplementary Methods, Supplementary Table 3 and Supplementary References.
Supplementary Table 1
Comparison of numbers of significantly differentially regulated genes.
Supplementary Table 2
Gene expression in 35S::MtCLE53 and 35S::GUS roots.
Rights and permissions
About this article
Cite this article
Müller, L.M., Flokova, K., Schnabel, E. et al. A CLE–SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza. Nat. Plants 5, 933–939 (2019). https://doi.org/10.1038/s41477-019-0501-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41477-019-0501-1
This article is cited by
-
Strigolactones in Plants: From Development to Abiotic Stress Management
Journal of Plant Growth Regulation (2024)
-
Modulation of plant immunity and biotic interactions under phosphate deficiency
Journal of Plant Research (2024)
-
A Mutation in Mediator Subunit MED16A Suppresses Nodulation and Increases Arbuscule Density in Medicago truncatula
Journal of Plant Growth Regulation (2023)
-
Proteomdynamik im Gefäßsystem von Pflanzen
BIOspektrum (2023)
-
Physiological and transcriptomic response of Medicago truncatula to colonization by high- or low-benefit arbuscular mycorrhizal fungi
Mycorrhiza (2022)