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A transposon surveillance mechanism that safeguards plant male fertility during stress

Subjects

Abstract

Although plants are able to withstand a range of environmental conditions, spikes in ambient temperature can impact plant fertility causing reductions in seed yield and notable economic losses1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production3. Here, we identified two Argonaute-like proteins whose activities are required to sustain male fertility in maize plants under high temperatures. We found that MALE-ASSOCIATED ARGONAUTE-1 and -2 associate with temperature-induced phased secondary small RNAs in pre-meiotic anthers and are essential to controlling the activity of retrotransposons in male meiocyte initials. Biochemical and structural analyses revealed how male-associated Argonaute activity and its interaction with retrotransposon RNA targets is modulated through the dynamic phosphorylation of a set of highly conserved, surface-located serine residues. Our results demonstrate that an Argonaute-dependent, RNA-guided surveillance mechanism is critical in plants to sustain male fertility under environmentally constrained conditions, by controlling the mutagenic activity of transposons in male germ cells.

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Fig. 1: MAGO and pre-meiotic sRNAs are essential for male fertility in maize.
Fig. 2: MAGO1/2 are necessary to silence stress-activated retrotransposons in maize male germ cells.
Fig. 3: MAGO activity is modulated by dynamic changes in phosphorylation induced by heat stress.

Data availability

Sequence data (messenger RNA-seq, nanoPARE-seq, sRNA-seq and LTR-seq) that support the findings of this study have been deposited at the European Nucleotide Archive under accession code ERP118841. Mass spectrometry proteomics data have been deposited at the ProteomeXchange Consortium with the dataset identifier PXD013891.

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Acknowledgements

We thank G. Grant and P. Watson for help with plant husbandry, L. M. Costa for discussions and comments on the manuscript and N. Springer and S. Anderson for help with transposon analysis. This research was supported by awards from the US National Science Foundation (nos. 1027445 to A.W.S. and 1649424 and 1754097 to B.C.M.), European Research Council (grant no. 637888 to M.D.N.) and Biotechnology and Biological Sciences Research Council (BBSRC) (nos. BB/L003023/1, BB/N005279/1, BB/N00194X/1 and BB/P02601X/1 to J.G.-M).

Author information

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Authors

Contributions

Y.-S.L. and R.M. cultivated plants, harvested samples and collected phenotypic data. R.P., J.G.-M. and J.R. identified transposon insertions. J.D. performed phosphoproteome analysis. R.M. and Y.-S.L. performed immunoprecipitation and sRNA-seq libraries. A.L. and J.C.L. generated constructs and transgenic lines for HC-Pro and HDZIV6 transactivation. R.P. constructed nanoPARE libraries. R.M., A.D., S.T., S.A. and M.D.N. performed bioinformatic analysis. C.d.G. performed molecular dynamics simulation and protein modelling. Y.-S.L., R.M., J.D., A.D., S.T. and C.d.G. prepared figures and tables. A.W.S., J.B., B.C.M., M.D.N., J.R. and J.G.-M. co-ordinated experiments. Y.-S.L., R.M. and J.G.-M. conceived the project. J.G.-M. wrote the manuscript with input from the rest of the authors.

Corresponding author

Correspondence to Jose Gutierrez-Marcos.

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Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–13 and source data with supporting blots and/or gels.

Reporting Summary

Supplementary Table 1

List of differentially expressed Hphasi loci.

Supplementary Table 2

List of differentially expressed genes in pre-meiotic anthers from wild-type and MAGOKD plants.

Supplementary Table 3

List of differentially expressed transposons in pre-meiotic anthers from wild-type and MAGOKD plants.

Supplementary Table 4

List of predicted retrotransposons (LTRs) targeted by Hphasi.

Supplementary Table 5

List of new transposon insertions determined by LTR-seq.

Supplementary Table 6

List of differentially accumulated phosphopeptides from pre-meiotic anthers of wild-type plants exposed to heat stress.

Supplementary Table 7

Conservation of phosphorylated serine and threonine residues in different Argonautes.

Supplementary Table 8

List of oligonucleotides and synthetic DNA constructs.

Supplementary Table 9

Next-generation sequencing library details.

Supplementary Video 1

Electrostatic potential distribution on the molecular surface of the central cleft of native and phosphorylated MAGO2.

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Lee, YS., Maple, R., Dürr, J. et al. A transposon surveillance mechanism that safeguards plant male fertility during stress. Nat. Plants 7, 34–41 (2021). https://doi.org/10.1038/s41477-020-00818-5

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