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 C. Lamb; Stefano Amantia; Anne W. Sylvester; James A. Birchler; Blake C. Meyers; Michael D. 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 C. Lamb, Stefano Amantia, Anne W. Sylvester, James A. Birchler, Blake C. Meyers, Michael D. Nodine, Jacques Rouster, Jose Gutierrez-Marcos

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23 Scopus citations

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 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.

Original language	English
Pages (from-to)	34-41
Number of pages	8
Journal	Nature Plants
Volume	7
Issue number	1
DOIs	https://doi.org/10.1038/s41477-020-00818-5
State	Published - Jan 2021

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Lee, Y. S., Maple, R., Dürr, J., Dawson, A., Tamim, S., del Genio, C., Papareddy, R., Luo, A., Lamb, J. C., Amantia, S., Sylvester, A. W., Birchler, J. A., Meyers, B. C., Nodine, M. D., Rouster, J., & Gutierrez-Marcos, J. (2021). A transposon surveillance mechanism that safeguards plant male fertility during stress. Nature Plants, 7(1), 34-41. https://doi.org/10.1038/s41477-020-00818-5

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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 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.",

author = "Lee, {Yang Seok} 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 Lamb, {Jonathan C.} and Stefano Amantia and Sylvester, {Anne W.} and Birchler, {James A.} and Meyers, {Blake C.} and Nodine, {Michael D.} and Jacques Rouster and Jose Gutierrez-Marcos",

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year = "2021",

month = jan,

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

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Lee, YS, Maple, R, Dürr, J, Dawson, A, Tamim, S, del Genio, C, Papareddy, R, Luo, A, Lamb, JC, Amantia, S, Sylvester, AW, Birchler, JA, Meyers, BC, Nodine, MD, Rouster, J & Gutierrez-Marcos, J 2021, 'A transposon surveillance mechanism that safeguards plant male fertility during stress', Nature Plants, vol. 7, no. 1, pp. 34-41. https://doi.org/10.1038/s41477-020-00818-5

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AU - Lee, Yang Seok

AU - Maple, Robert

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AU - Dawson, Alexander

AU - Tamim, Saleh

AU - del Genio, Charo

AU - Papareddy, Ranjith

AU - Luo, Anding

AU - Lamb, Jonathan C.

AU - Amantia, Stefano

AU - Sylvester, Anne W.

AU - Birchler, James A.

AU - Meyers, Blake C.

AU - Nodine, Michael D.

AU - Rouster, Jacques

AU - Gutierrez-Marcos, Jose

PY - 2021/1

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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 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.

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 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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A transposon surveillance mechanism that safeguards plant male fertility during stress

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