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Convergence of sphingolipid desaturation across over 500 million years of plant evolution

Abstract

For plants, acclimation to low temperatures is fundamental to survival. This process involves the modification of lipids to maintain membrane fluidity. We previously identified a new cold-induced putative desaturase in Physcomitrium (Physcomitrella) patens. Lipid profiles of null mutants of this gene lack sphingolipids containing monounsaturated C24 fatty acids, classifying the new protein as sphingolipid fatty acid denaturase (PpSFD). PpSFD mutants showed a cold-sensitive phenotype as well as higher susceptibility to the oomycete Pythium, assigning functions in stress tolerance for PpSFD. Ectopic expression of PpSFD in the Atads2.1 (acyl coenzyme A desaturase-like 2) Arabidopsis thaliana mutant functionally complemented its cold-sensitive phenotype. While these two enzymes catalyse a similar reaction, their evolutionary origin is clearly different since AtADS2 is a methyl-end desaturase whereas PpSFD is a cytochrome b5 fusion desaturase. Altogether, we suggest that adjustment of membrane fluidity evolved independently in mosses and seed plants, which diverged more than 500 million years ago.

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Fig. 1: Two types of membrane-bound desaturases exist in plants.
Fig. 2: Analysis of PpSFD activity in P. patens and S. cerevisiae.
Fig. 3: Relative changes in the lipid composition after cold stress in wild type and Ppsfd mutant.
Fig. 4: Phenotype of P. patens wild type and Ppsfd mutants.
Fig. 5: Cold-stress experiment with A. thaliana.
Fig. 6: Ppsfd mutants are sensitive against the oomycete Pythium.
Fig. 7: A phylogenetic framework for the origin of PpSFD.

Data availability

All moss mutants described here were deposited in the International Moss Stock Center (IMSC, http://www.moss-stock-center.org/). The IMSC numbers for the confirmed knockouts are 40561 (gKO25 3), 40568 (gKO25 10) and 40569 (gKO25 11). Source data are provided with this paper.

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Acknowledgements

We thank P. Meyer and S. Freitag (Göttingen) for technical assistance, D. Trautmann (Freiburg) for help with carotinoid profiling, A. Hartenhauer (Dresden) for help with the infection experiments, L. Mohnike (Göttingen) for help with the art work and T. Haslam (Göttingen) for critical reading of the manuscript. H.C.R. and J.G. were supported by the Microbiology and Biochemistry programme of Göttingen Graduate Center for Neurosciences, Biophysics, and Molecular Biosciences (GGNB). I.F. acknowledges funding through the German Research Foundation (DFG: INST 186/822-1, INST 186/1167-1 and ZUK 45/2010). R.R. acknowledges funding from the Excellence Initiative of the German Federal and State Governments (EXC 294 and CIBSS – EXC-2189 – Project ID 390939984). J.d.V. is supported through funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant no. 852725; ERC Starting Grant ‘TerreStriAL’).

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Contributions

R.R., J. Markham, J.L.M. and I.F. designed the study. H.C.R., C.H., K.F., E.H., A.K.O. and J. Mittag undertook the experiments. H.C.R., C.H., K.F., J.L.M., J.G., J. Markham, J. Mittag, N.v.G., J.d.V., R.R. and I.F. analysed the data. H.C.R., K.F., J.d.V., R.R. and I.F. wrote the paper. All authors read, commented on and approved the final version of the manuscript.

Corresponding authors

Correspondence to Ralf Reski or Ivo Feussner.

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Peer review information Nature Plants thanks Sebastien Mongrand, Jay Thelen and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–15 and Tables 1 and 2.

Reporting Summary

Supplementary Data

Supplementary Fig. 2, uncropped and unprocessed full scans; Supplementary Fig. 4, growth rate in liquid media; Supplementary Fig. 5, fatty acid profile; Supplementary Fig. 6, carotenoid profiles from gametophores of P. patens; Supplementary Fig. 7, ceramide profile; Supplementary Figs. 8–12, detected lipid species (relative peak areas of all detected molecular lipid species); Supplementary Fig. 13, relative transcript levels of genes AtADS2 and PpSFD in different cold-stressed A. thaliana complementation lines; Supplementary Fig. 14, relative peak areas of all detected lipid molecular species of A. thaliana plants.

Source data

Source Data Fig. 2

Data sheet for a,b, detected lipid species (relative peak areas of all detected molecular lipid species); data sheet for c, Cer profiles of yeasts (ceramide profiles of transgenic S. cerevisiae lines).

Source Data Fig. 3

Data sheet for a, total lipid peak areas (absolute total peak areas of lipid class [cps] → fold changes); data sheet for b, detected lipid species (relative peak areas of all detected molecular lipid species → relative lipid amount regarding fatty acid composition).

Source Data Fig. 4

Chlorophyll content.

Source Data Fig. 5

Data sheet for a, cold-stress photos (images and weight of A. thaliana plants before and after cold stress.); data sheet for b, relative transcript levels of genes AtADS2 and PpSFD in different cold-stressed A. thaliana complementation lines; data sheet for c, SF 5.2 cold-stress lipid data (relative peak areas of all detected lipid molecular species of A. thaliana plants).

Source Data Fig. 6

Pythium infection.

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Resemann, H.C., Herrfurth, C., Feussner, K. et al. Convergence of sphingolipid desaturation across over 500 million years of plant evolution. Nat. Plants 7, 219–232 (2021). https://doi.org/10.1038/s41477-020-00844-3

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