A transposon surveillance mechanism that safeguards plant male fertility during stress

Yang-Seok Lee; Robert Maple; Julius Dürr; Alexander Dawson; Saleh Tamim; Charo del Genio; Ranjith Papareddy; Anding Luo; Jonathan Lamb; Stefano Amantia; Anne Sylvester; James Birchler; Blake Meyers; Michael Nodine; Jacques Rouster; Jose Gutierrez-Marcos

doi:10.1038/s41477-020-00818-5

A transposon surveillance mechanism that safeguards plant male fertility during stress

Yang-Seok Lee, Robert Maple, Julius Dürr, Alexander Dawson, Saleh Tamim, Charo del Genio, Ranjith Papareddy, Anding Luo, Jonathan Lamb, Stefano Amantia, Anne Sylvester, James Birchler, Blake Meyers, Michael Nodine, Jacques Rouster, Jose Gutierrez-Marcos

Research output: Contribution to journal › Article › peer-review

2 Citations (Scopus)

4 Downloads (Pure)

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 losses ^1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production ³. 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.

Original language	English
Pages (from-to)	34-41
Number of pages	8
Journal	Nature Plants
Volume	7
DOIs	https://doi.org/10.1038/s41477-020-00818-5
Publication status	Published - 4 Jan 2021

Bibliographical note

Copyright © and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders.

Funder

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).

ASJC Scopus subject areas

Plant Science

Access to Document

10.1038/s41477-020-00818-5

Post-PrintAccepted author manuscript, 1.73 MB

https://www.biorxiv.org/content/10.1101/2020.10.03.324764v1

Cite this

Lee, Y-S., Maple, R., Dürr, J., Dawson, A., Tamim, S., del Genio, C., Papareddy, R., Luo, A., Lamb, J., Amantia, S., Sylvester, A., Birchler, J., Meyers, B., Nodine, M., Rouster, J., & Gutierrez-Marcos, J. (2021). A transposon surveillance mechanism that safeguards plant male fertility during stress. Nature Plants, 7, 34-41. https://doi.org/10.1038/s41477-020-00818-5

A transposon surveillance mechanism that safeguards plant male fertility during stress. / Lee, Yang-Seok; Maple, Robert; Dürr, Julius; Dawson, Alexander; Tamim, Saleh; del Genio, Charo; Papareddy, Ranjith; Luo, Anding; Lamb, Jonathan; Amantia, Stefano; Sylvester, Anne; Birchler, James; Meyers, Blake; Nodine, Michael; Rouster, Jacques; Gutierrez-Marcos, Jose.

In: Nature Plants, Vol. 7, 04.01.2021, p. 34-41.

Research output: Contribution to journal › Article › peer-review

Lee, Yang-Seok ; Maple, Robert ; Dürr, Julius ; Dawson, Alexander ; Tamim, Saleh ; del Genio, Charo ; Papareddy, Ranjith ; Luo, Anding ; Lamb, Jonathan ; Amantia, Stefano ; Sylvester, Anne ; Birchler, James ; Meyers, Blake ; Nodine, Michael ; Rouster, Jacques ; Gutierrez-Marcos, Jose. / A transposon surveillance mechanism that safeguards plant male fertility during stress. In: Nature Plants. 2021 ; Vol. 7. pp. 34-41.

@article{0f9f6a1f082d44aab6287e06dc58fb7e,

title = "A transposon surveillance mechanism that safeguards plant male fertility during stress",

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 losses 1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production 3. 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. ",

author = "Yang-Seok Lee and Robert Maple and Julius D{\"u}rr and Alexander Dawson and Saleh Tamim and {del Genio}, Charo and Ranjith Papareddy and Anding Luo and Jonathan Lamb and Stefano Amantia and Anne Sylvester and James Birchler and Blake Meyers and Michael Nodine and Jacques Rouster and Jose Gutierrez-Marcos",

note = "Copyright {\textcopyright} and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. ",

year = "2021",

month = jan,

day = "4",

doi = "10.1038/s41477-020-00818-5",

language = "English",

volume = "7",

pages = "34--41",

journal = "Nature Plants",

issn = "2055-0278",

publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - A transposon surveillance mechanism that safeguards plant male fertility during stress

AU - Lee, Yang-Seok

AU - Maple, Robert

AU - Dürr, Julius

AU - Dawson, Alexander

AU - Tamim, Saleh

AU - del Genio, Charo

AU - Papareddy, Ranjith

AU - Luo, Anding

AU - Lamb, Jonathan

AU - Amantia, Stefano

AU - Sylvester, Anne

AU - Birchler, James

AU - Meyers, Blake

AU - Nodine, Michael

AU - Rouster, Jacques

AU - Gutierrez-Marcos, Jose

N1 - Copyright © and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders.

PY - 2021/1/4

Y1 - 2021/1/4

N2 - 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 losses 1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production 3. 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.

AB - 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 losses 1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production 3. 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.

UR - https://charodelgenio.weebly.com/mago.html

UR - https://www.youtube.com/watch?v=puKDIYSSH3U

UR - http://www.scopus.com/inward/record.url?scp=85098779339&partnerID=8YFLogxK

U2 - 10.1038/s41477-020-00818-5

DO - 10.1038/s41477-020-00818-5

M3 - Article

VL - 7

SP - 34

EP - 41

JO - Nature Plants

JF - Nature Plants

SN - 2055-0278

ER -

A transposon surveillance mechanism that safeguards plant male fertility during stress

Abstract

Bibliographical note

Funder

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this