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The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark

During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development...

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Autores principales: Rovira, Arnau, Sentandreu, Maria, Nagatani, Akira, Leivar, Pablo, Monte, Elena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985339/
https://www.ncbi.nlm.nih.gov/pubmed/33767720
http://dx.doi.org/10.3389/fpls.2021.636098
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author Rovira, Arnau
Sentandreu, Maria
Nagatani, Akira
Leivar, Pablo
Monte, Elena
author_facet Rovira, Arnau
Sentandreu, Maria
Nagatani, Akira
Leivar, Pablo
Monte, Elena
author_sort Rovira, Arnau
collection PubMed
description During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development in the dark after seedling emergence from the seed follows three distinctly timed and sequential phases: formation, maintenance, and eventual opening. We previously identified MISREGULATED IN DARK9 (MIDA9) as a phytochrome interacting factor (PIF)-repressed gene in the dark necessary for hook development during etiolated growth. MIDA9 encodes the type 2C phosphatase PP2C.D1, and pp2c-d1/mida9 mutants exhibit open hooks in the dark. Recent evidence has described that PP2C.D1 and other PP2C.D members negatively regulate SMALL AUXIN UP RNA (SAUR)-mediated cell elongation. However, the fundamental question of the timing of PP2C.D1 action (and possibly other members of the PP2C.D family) during hook development remains to be addressed. Here, we show that PP2C.D1 is required immediately after germination to form the hook. pp2c.d1/mida9 shows reduced cell expansion in the outer layer of the hook and, therefore, does not establish the differential cell growth necessary for hook formation, indicating that PP2C.D1 is necessary to promote cell elongation during this early stage. Additionally, genetic analyses of single and high order mutants in PP2C.D1, PP2C.D2, and PP2C.D5 demonstrate that the three PP2C.Ds act collectively and sequentially during etiolation: whereas PP2C.D1 dominates hook formation, PP2C.D2 is necessary during the maintenance phase, and PP2C.D5 acts to prevent opening during the third phase together with PP2C.D1 and PP2C.D2. Finally, we uncover a possible connection of PP2C.D1 levels with ethylene physiology, which could help optimize hook formation during post-germinative growth in the dark.
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spelling pubmed-79853392021-03-24 The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark Rovira, Arnau Sentandreu, Maria Nagatani, Akira Leivar, Pablo Monte, Elena Front Plant Sci Plant Science During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development in the dark after seedling emergence from the seed follows three distinctly timed and sequential phases: formation, maintenance, and eventual opening. We previously identified MISREGULATED IN DARK9 (MIDA9) as a phytochrome interacting factor (PIF)-repressed gene in the dark necessary for hook development during etiolated growth. MIDA9 encodes the type 2C phosphatase PP2C.D1, and pp2c-d1/mida9 mutants exhibit open hooks in the dark. Recent evidence has described that PP2C.D1 and other PP2C.D members negatively regulate SMALL AUXIN UP RNA (SAUR)-mediated cell elongation. However, the fundamental question of the timing of PP2C.D1 action (and possibly other members of the PP2C.D family) during hook development remains to be addressed. Here, we show that PP2C.D1 is required immediately after germination to form the hook. pp2c.d1/mida9 shows reduced cell expansion in the outer layer of the hook and, therefore, does not establish the differential cell growth necessary for hook formation, indicating that PP2C.D1 is necessary to promote cell elongation during this early stage. Additionally, genetic analyses of single and high order mutants in PP2C.D1, PP2C.D2, and PP2C.D5 demonstrate that the three PP2C.Ds act collectively and sequentially during etiolation: whereas PP2C.D1 dominates hook formation, PP2C.D2 is necessary during the maintenance phase, and PP2C.D5 acts to prevent opening during the third phase together with PP2C.D1 and PP2C.D2. Finally, we uncover a possible connection of PP2C.D1 levels with ethylene physiology, which could help optimize hook formation during post-germinative growth in the dark. Frontiers Media S.A. 2021-03-09 /pmc/articles/PMC7985339/ /pubmed/33767720 http://dx.doi.org/10.3389/fpls.2021.636098 Text en Copyright © 2021 Rovira, Sentandreu, Nagatani, Leivar and Monte. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Rovira, Arnau
Sentandreu, Maria
Nagatani, Akira
Leivar, Pablo
Monte, Elena
The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title_full The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title_fullStr The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title_full_unstemmed The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title_short The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
title_sort sequential action of mida9/pp2c.d1, pp2c.d2, and pp2c.d5 is necessary to form and maintain the hook after germination in the dark
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985339/
https://www.ncbi.nlm.nih.gov/pubmed/33767720
http://dx.doi.org/10.3389/fpls.2021.636098
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