LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance

Elodie Billey; Said Hafidh; Isabel Cruz-gallardo; Celso G. Litholdo; Viviane Jean; Marie-Christine Carpentier; Claire Picart; Vinod Kumar; Katarina Kulichova; Eric Maréchal; David Honys; Maria R. Conte; Jean-Marc Deragon; Cécile Bousquet-Antonelli

doi:10.1093/plcell/koab131

LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance

Elodie Billey
, Said Hafidh
, Isabel Cruz-gallardo
, Celso G. Litholdo
, Viviane Jean
, Marie-Christine Carpentier
, Claire Picart
, Vinod Kumar
, Katarina Kulichova
, Eric Maréchal
, David Honys
, Maria R. Conte
, Jean-Marc Deragon
, Cécile Bousquet-Antonelli

Laboratoire Génome et Développement des Plantes, UMR5096, Université de Perpignan Via Domitia, 66860 Perpignan, France
Czech Academy of Sciences
King's College London, Randall Centre for Cell and Molecular Biophysics, London SE1 1UL, UK. [email protected].
Laboratoire de Physiologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRAE, Université Grenoble Alpes, IRIG, CEA Grenoble, 38054 Grenoble, France
Institut Universitaire de France, 75231 Paris Cedex 5, France
Laboratoire Génome et Développement des Plantes, UMR5096, CNRS, 66860 Perpignan, France

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

30 Citations (Scopus)

Abstract

Increasing evidence suggests that posttranscriptional regulation is a key player in the transition between mature pollen and the progamic phase (from pollination to fertilization). Nonetheless, the actors in this messenger RNA (mRNA)-based gene expression reprogramming are poorly understood. We demonstrate that the evolutionarily conserved RNA-binding protein LARP6C is necessary for the transition from dry pollen to pollen tubes and the guided growth of pollen tubes towards the ovule in Arabidopsis thaliana. In dry pollen, LARP6C binds to transcripts encoding proteins that function in lipid synthesis and homeostasis, vesicular trafficking, and polarized cell growth. LARP6C also forms cytoplasmic granules that contain the poly(A) binding protein and possibly represent storage sites for translationally silent mRNAs. In pollen tubes, the loss of LARP6C negatively affects the quantities and distribution of storage lipids, as well as vesicular trafficking. In Nicotiana benthamiana leaf cells and in planta, analysis of reporter mRNAs designed from the LARP6C target MGD2 provided evidence that LARP6C can shift from a repressor to an activator of translation when the pollen grain enters the progamic phase. We propose that LARP6C orchestrates the timely posttranscriptional regulation of a subset of mRNAs in pollen during the transition from the quiescent to active state and along the progamic phase to promote male fertilization in plants.

Original language	English
Pages (from-to)	2637-2661
Number of pages	25
Journal	Plant Cell
Volume	33
Issue number	8
Early online date	17 May 2021
DOIs	https://doi.org/10.1093/plcell/koab131
Publication status	Published - Aug 2021

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10.1093/plcell/koab131

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Billey, E., Hafidh, S., Cruz-gallardo, I., Litholdo, C. G., Jean, V., Carpentier, M.-C., Picart, C., Kumar, V., Kulichova, K., Maréchal, E., Honys, D., Conte, M. R., Deragon, J.-M., & Bousquet-Antonelli, C. (2021). LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance. Plant Cell, 33(8), 2637-2661. https://doi.org/10.1093/plcell/koab131

@article{19402ae052c24254a1028bd3668f7f9c,

title = "LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance",

abstract = "Increasing evidence suggests that posttranscriptional regulation is a key player in the transition between mature pollen and the progamic phase (from pollination to fertilization). Nonetheless, the actors in this messenger RNA (mRNA)-based gene expression reprogramming are poorly understood. We demonstrate that the evolutionarily conserved RNA-binding protein LARP6C is necessary for the transition from dry pollen to pollen tubes and the guided growth of pollen tubes towards the ovule in Arabidopsis thaliana. In dry pollen, LARP6C binds to transcripts encoding proteins that function in lipid synthesis and homeostasis, vesicular trafficking, and polarized cell growth. LARP6C also forms cytoplasmic granules that contain the poly(A) binding protein and possibly represent storage sites for translationally silent mRNAs. In pollen tubes, the loss of LARP6C negatively affects the quantities and distribution of storage lipids, as well as vesicular trafficking. In Nicotiana benthamiana leaf cells and in planta, analysis of reporter mRNAs designed from the LARP6C target MGD2 provided evidence that LARP6C can shift from a repressor to an activator of translation when the pollen grain enters the progamic phase. We propose that LARP6C orchestrates the timely posttranscriptional regulation of a subset of mRNAs in pollen during the transition from the quiescent to active state and along the progamic phase to promote male fertilization in plants.",

author = "Elodie Billey and Said Hafidh and Isabel Cruz-gallardo and Litholdo, \{Celso G.\} and Viviane Jean and Marie-Christine Carpentier and Claire Picart and Vinod Kumar and Katarina Kulichova and Eric Mar{\'e}chal and David Honys and Conte, \{Maria R.\} and Jean-Marc Deragon and C{\'e}cile Bousquet-Antonelli",

note = "Funding Information: This work was funded by the CNRS, The University of Perpignan (UPVD), the Agence Nationale pour la Recherche (ANR) grant Heat-EpiRNA (grant no. ANR-17-CE20-007-01); a Bonus Quality Research (BQR) funded by the University of Perpignan; a Collaborative PICS Project (LARP\&STRESS, grant no. 6170) funded by CNRS; Grantov? agentura Cesk? republiky (GACR; grant nos. 17-23203S and 18-02448S), European Regional Development Fund-Project ?Centre for Experimental Plant Biology? (No. CZ.02.1.01/0.0/0.0/16\_019/ 0000738) and the Royal Society Newton International fellowship (ref. NF140482). This study is set within the framework of the ?Laboratoires d?Excellence (LABEX)? TULIP (ANR-10LABX-41). E.B. was the recipient of a PhD grant from the UPVD, Doctoral School ED305. C.G.L. Jr is the recipient of a short-term contract supported by the ANR Heat-EpiRNA (ANR-17-CE20-007-01). S.H., K.K., and D.H. are supported by GACR (grant nos. 17-23203S and 18-02448S). S.H. is also supported by European Regional Development Fund-Project ?Centre for Experimental Plant Biology? (grant no. CZ.02.1.01/0.0/0.0/16\_019/0000738). I.C.G. was supported by a Royal Society Newton International fellowship (ref. NF140482). I.G.C. and M.R.C. thank the Centre for Biomolecular Spectroscopy at King?s College London funded by a capital award from the Wellcome Trust. Funding Information: This work was funded by the CNRS, The University of Perpignan (UPVD), the Agence Nationale pour la Recherche (ANR) grant Heat-EpiRNA (grant no. ANR-17-CE20-007-01); a Bonus Quality Research (BQR) funded by the University of Perpignan; a Collaborative PICS Project (LARP\&STRESS, grant no. 6170) funded by CNRS; Grantov{\'a} agentura Ce≤ sk{\'e} republiky (GACR; grant nos. 17-23203S and 18-02448S), European Regional Development Fund-Project “Centre for Experimental Plant Biology” (No. CZ.02.1.01/0.0/0.0/16\_019/ 0000738) and the Royal Society Newton International fellowship (ref. NF140482). This study is set within the framework of the “Laboratoires d{\textquoteright}Excellence (LABEX)” TULIP (ANR-10-LABX-41). E.B. was the recipient of a PhD grant from the UPVD, Doctoral School ED305. C.G.L. Jr is the recipient of a short-term contract supported by the ANR Heat-EpiRNA (ANR-17-CE20-007-01). S.H., K.K., and D.H. are supported by GACR (grant nos. 17-23203S and 18-02448S). S.H. is also supported by European Regional Development Fund-Project “Centre for Experimental Plant Biology” (grant no. CZ.02.1.01/0.0/0.0/16\_019/0000738). I.C.G. was supported by a Royal Society Newton International fellowship (ref. NF140482). I.G.C. and M.R.C. thank the Centre for Biomolecular Spectroscopy at King{\textquoteright}s College London funded by a capital award from the Wellcome Trust. Publisher Copyright: {\textcopyright} American Society of Plant Biologists 2021. All rights reserved. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = aug,

doi = "10.1093/plcell/koab131",

language = "English",

volume = "33",

pages = "2637--2661",

journal = "Plant Cell",

issn = "1040-4651",

publisher = "American Society of Plant Biologists",

number = "8",

}

Billey, E, Hafidh, S, Cruz-gallardo, I, Litholdo, CG, Jean, V, Carpentier, M-C, Picart, C, Kumar, V, Kulichova, K, Maréchal, E, Honys, D, Conte, MR, Deragon, J-M & Bousquet-Antonelli, C 2021, 'LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance', Plant Cell, vol. 33, no. 8, pp. 2637-2661. https://doi.org/10.1093/plcell/koab131

TY - JOUR

T1 - LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance

AU - Billey, Elodie

AU - Hafidh, Said

AU - Cruz-gallardo, Isabel

AU - Litholdo, Celso G.

AU - Jean, Viviane

AU - Carpentier, Marie-Christine

AU - Picart, Claire

AU - Kumar, Vinod

AU - Kulichova, Katarina

AU - Maréchal, Eric

AU - Honys, David

AU - Conte, Maria R.

AU - Deragon, Jean-Marc

AU - Bousquet-Antonelli, Cécile

N1 - Funding Information: This work was funded by the CNRS, The University of Perpignan (UPVD), the Agence Nationale pour la Recherche (ANR) grant Heat-EpiRNA (grant no. ANR-17-CE20-007-01); a Bonus Quality Research (BQR) funded by the University of Perpignan; a Collaborative PICS Project (LARP&STRESS, grant no. 6170) funded by CNRS; Grantov? agentura Cesk? republiky (GACR; grant nos. 17-23203S and 18-02448S), European Regional Development Fund-Project ?Centre for Experimental Plant Biology? (No. CZ.02.1.01/0.0/0.0/16_019/ 0000738) and the Royal Society Newton International fellowship (ref. NF140482). This study is set within the framework of the ?Laboratoires d?Excellence (LABEX)? TULIP (ANR-10LABX-41). E.B. was the recipient of a PhD grant from the UPVD, Doctoral School ED305. C.G.L. Jr is the recipient of a short-term contract supported by the ANR Heat-EpiRNA (ANR-17-CE20-007-01). S.H., K.K., and D.H. are supported by GACR (grant nos. 17-23203S and 18-02448S). S.H. is also supported by European Regional Development Fund-Project ?Centre for Experimental Plant Biology? (grant no. CZ.02.1.01/0.0/0.0/16_019/0000738). I.C.G. was supported by a Royal Society Newton International fellowship (ref. NF140482). I.G.C. and M.R.C. thank the Centre for Biomolecular Spectroscopy at King?s College London funded by a capital award from the Wellcome Trust. Funding Information: This work was funded by the CNRS, The University of Perpignan (UPVD), the Agence Nationale pour la Recherche (ANR) grant Heat-EpiRNA (grant no. ANR-17-CE20-007-01); a Bonus Quality Research (BQR) funded by the University of Perpignan; a Collaborative PICS Project (LARP&STRESS, grant no. 6170) funded by CNRS; Grantová agentura Ce≤ ské republiky (GACR; grant nos. 17-23203S and 18-02448S), European Regional Development Fund-Project “Centre for Experimental Plant Biology” (No. CZ.02.1.01/0.0/0.0/16_019/ 0000738) and the Royal Society Newton International fellowship (ref. NF140482). This study is set within the framework of the “Laboratoires d’Excellence (LABEX)” TULIP (ANR-10-LABX-41). E.B. was the recipient of a PhD grant from the UPVD, Doctoral School ED305. C.G.L. Jr is the recipient of a short-term contract supported by the ANR Heat-EpiRNA (ANR-17-CE20-007-01). S.H., K.K., and D.H. are supported by GACR (grant nos. 17-23203S and 18-02448S). S.H. is also supported by European Regional Development Fund-Project “Centre for Experimental Plant Biology” (grant no. CZ.02.1.01/0.0/0.0/16_019/0000738). I.C.G. was supported by a Royal Society Newton International fellowship (ref. NF140482). I.G.C. and M.R.C. thank the Centre for Biomolecular Spectroscopy at King’s College London funded by a capital award from the Wellcome Trust. Publisher Copyright: © American Society of Plant Biologists 2021. All rights reserved. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/8

Y1 - 2021/8

N2 - Increasing evidence suggests that posttranscriptional regulation is a key player in the transition between mature pollen and the progamic phase (from pollination to fertilization). Nonetheless, the actors in this messenger RNA (mRNA)-based gene expression reprogramming are poorly understood. We demonstrate that the evolutionarily conserved RNA-binding protein LARP6C is necessary for the transition from dry pollen to pollen tubes and the guided growth of pollen tubes towards the ovule in Arabidopsis thaliana. In dry pollen, LARP6C binds to transcripts encoding proteins that function in lipid synthesis and homeostasis, vesicular trafficking, and polarized cell growth. LARP6C also forms cytoplasmic granules that contain the poly(A) binding protein and possibly represent storage sites for translationally silent mRNAs. In pollen tubes, the loss of LARP6C negatively affects the quantities and distribution of storage lipids, as well as vesicular trafficking. In Nicotiana benthamiana leaf cells and in planta, analysis of reporter mRNAs designed from the LARP6C target MGD2 provided evidence that LARP6C can shift from a repressor to an activator of translation when the pollen grain enters the progamic phase. We propose that LARP6C orchestrates the timely posttranscriptional regulation of a subset of mRNAs in pollen during the transition from the quiescent to active state and along the progamic phase to promote male fertilization in plants.

AB - Increasing evidence suggests that posttranscriptional regulation is a key player in the transition between mature pollen and the progamic phase (from pollination to fertilization). Nonetheless, the actors in this messenger RNA (mRNA)-based gene expression reprogramming are poorly understood. We demonstrate that the evolutionarily conserved RNA-binding protein LARP6C is necessary for the transition from dry pollen to pollen tubes and the guided growth of pollen tubes towards the ovule in Arabidopsis thaliana. In dry pollen, LARP6C binds to transcripts encoding proteins that function in lipid synthesis and homeostasis, vesicular trafficking, and polarized cell growth. LARP6C also forms cytoplasmic granules that contain the poly(A) binding protein and possibly represent storage sites for translationally silent mRNAs. In pollen tubes, the loss of LARP6C negatively affects the quantities and distribution of storage lipids, as well as vesicular trafficking. In Nicotiana benthamiana leaf cells and in planta, analysis of reporter mRNAs designed from the LARP6C target MGD2 provided evidence that LARP6C can shift from a repressor to an activator of translation when the pollen grain enters the progamic phase. We propose that LARP6C orchestrates the timely posttranscriptional regulation of a subset of mRNAs in pollen during the transition from the quiescent to active state and along the progamic phase to promote male fertilization in plants.

UR - https://www.scopus.com/pages/publications/85114190592

U2 - 10.1093/plcell/koab131

DO - 10.1093/plcell/koab131

M3 - Article

SN - 1040-4651

VL - 33

SP - 2637

EP - 2661

JO - Plant Cell

JF - Plant Cell

IS - 8

ER -

LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance

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