SeedTransNet: A directional translational network revealing regulatory patterns during seed maturation and germination

Bing Bai; Bastian Schiffthaler; Sjors van der Horst; Leo Willems; Alexander Vergara; Jacob Karström; Niklas Mähler; Nicolas Delhomme; Leónie Bentsink; Johannes Hanson

doi:10.1093/jxb/erac394

SeedTransNet: A directional translational network revealing regulatory patterns during seed maturation and germination

Bing Bai
, Bastian Schiffthaler
, Sjors van der Horst
, Leo Willems
, Alexander Vergara
, Jacob Karström
, Niklas Mähler
, Nicolas Delhomme
, Leónie Bentsink
, Johannes Hanson^*

^*Corresponding author for this work

Molecular Plant Physiology

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

Abstract

Seed maturation is the developmental process that prepares the embryo for the desiccated waiting period before germination. It is associated with a series of physiological changes leading to the establishment of seed dormancy, seed longevity, and desiccation tolerance. We studied translational changes during seed maturation and observed a gradual reduction in global translation during seed maturation. Transcriptome and translatome profiling revealed specific reduction in the translation of thousands of genes. By including previously published data on germination and seedling establishment, a regulatory network based on polysome occupancy data was constructed: SeedTransNet. Network analysis predicted translational regulatory pathways involving hundreds of genes with distinct functions. The network identified specific transcript sequence features suggesting separate translational regulatory circuits. The network revealed several seed maturation-associated genes as central nodes, and this was confirmed by specific seed phenotypes of the respective mutants. One of the regulators identified, an AWPM19 family protein, PM19-Like1 (PM19L1), was shown to regulate seed dormancy and longevity. This putative RNA-binding protein also affects the translational regulation of its target mRNA, as identified by SeedTransNet. Our data show the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions.

Original language	English
Pages (from-to)	2416–2432
Number of pages	17
Journal	Journal of Experimental Botany
Volume	74
Issue number	7
Early online date	8 Oct 2022
DOIs	https://doi.org/10.1093/jxb/erac394
Publication status	Published - 9 Apr 2023

Bibliographical note

Funding Information:
We thank Service XS, Leiden,The Netherlands for performing the microarray hybridizations. We also thank Mariana Aline Silva Artur for providing the PM19L1 overexpression line for validation of the seed longevity phenotype. We thank the UPSC Bioinformatics Facility for data handling, storage and analysis.We acknowledge the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science for access to the HPC2N and UPPMAX computational infrastructure. This work was supported by the Netherlands Organization for Scientific Research. BB was a recipient of a Kempe Fellowship. We thank Bio4Energy, a Strategic Research Environment appointed by the Swedish government, for supporting this work.

Publisher Copyright:
© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology.

Keywords

Arabidopsis thaliana
mRNA regulation
ribosome
seed germination
seed maturation
translatome profiling

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erac394Final published version, 2.5 MBLicence: CC BY

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title = "SeedTransNet: A directional translational network revealing regulatory patterns during seed maturation and germination",

abstract = "Seed maturation is the developmental process that prepares the embryo for the desiccated waiting period before germination. It is associated with a series of physiological changes leading to the establishment of seed dormancy, seed longevity, and desiccation tolerance. We studied translational changes during seed maturation and observed a gradual reduction in global translation during seed maturation. Transcriptome and translatome profiling revealed specific reduction in the translation of thousands of genes. By including previously published data on germination and seedling establishment, a regulatory network based on polysome occupancy data was constructed: SeedTransNet. Network analysis predicted translational regulatory pathways involving hundreds of genes with distinct functions. The network identified specific transcript sequence features suggesting separate translational regulatory circuits. The network revealed several seed maturation-associated genes as central nodes, and this was confirmed by specific seed phenotypes of the respective mutants. One of the regulators identified, an AWPM19 family protein, PM19-Like1 (PM19L1), was shown to regulate seed dormancy and longevity. This putative RNA-binding protein also affects the translational regulation of its target mRNA, as identified by SeedTransNet. Our data show the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions.",

keywords = "Arabidopsis thaliana, mRNA regulation, ribosome, seed germination, seed maturation, translatome profiling",

author = "Bing Bai and Bastian Schiffthaler and \{van der Horst\}, Sjors and Leo Willems and Alexander Vergara and Jacob Karstr{\"o}m and Niklas M{\"a}hler and Nicolas Delhomme and Le{\'o}nie Bentsink and Johannes Hanson",

note = "Funding Information: We thank Service XS, Leiden,The Netherlands for performing the microarray hybridizations. We also thank Mariana Aline Silva Artur for providing the PM19L1 overexpression line for validation of the seed longevity phenotype. We thank the UPSC Bioinformatics Facility for data handling, storage and analysis.We acknowledge the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science for access to the HPC2N and UPPMAX computational infrastructure. This work was supported by the Netherlands Organization for Scientific Research. BB was a recipient of a Kempe Fellowship. We thank Bio4Energy, a Strategic Research Environment appointed by the Swedish government, for supporting this work. Publisher Copyright: {\textcopyright} The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology.",

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AU - Bai, Bing

AU - Schiffthaler, Bastian

AU - van der Horst, Sjors

AU - Willems, Leo

AU - Vergara, Alexander

AU - Karström, Jacob

AU - Mähler, Niklas

AU - Delhomme, Nicolas

AU - Bentsink, Leónie

AU - Hanson, Johannes

N1 - Funding Information: We thank Service XS, Leiden,The Netherlands for performing the microarray hybridizations. We also thank Mariana Aline Silva Artur for providing the PM19L1 overexpression line for validation of the seed longevity phenotype. We thank the UPSC Bioinformatics Facility for data handling, storage and analysis.We acknowledge the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science for access to the HPC2N and UPPMAX computational infrastructure. This work was supported by the Netherlands Organization for Scientific Research. BB was a recipient of a Kempe Fellowship. We thank Bio4Energy, a Strategic Research Environment appointed by the Swedish government, for supporting this work. Publisher Copyright: © The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology.

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N2 - Seed maturation is the developmental process that prepares the embryo for the desiccated waiting period before germination. It is associated with a series of physiological changes leading to the establishment of seed dormancy, seed longevity, and desiccation tolerance. We studied translational changes during seed maturation and observed a gradual reduction in global translation during seed maturation. Transcriptome and translatome profiling revealed specific reduction in the translation of thousands of genes. By including previously published data on germination and seedling establishment, a regulatory network based on polysome occupancy data was constructed: SeedTransNet. Network analysis predicted translational regulatory pathways involving hundreds of genes with distinct functions. The network identified specific transcript sequence features suggesting separate translational regulatory circuits. The network revealed several seed maturation-associated genes as central nodes, and this was confirmed by specific seed phenotypes of the respective mutants. One of the regulators identified, an AWPM19 family protein, PM19-Like1 (PM19L1), was shown to regulate seed dormancy and longevity. This putative RNA-binding protein also affects the translational regulation of its target mRNA, as identified by SeedTransNet. Our data show the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions.

AB - Seed maturation is the developmental process that prepares the embryo for the desiccated waiting period before germination. It is associated with a series of physiological changes leading to the establishment of seed dormancy, seed longevity, and desiccation tolerance. We studied translational changes during seed maturation and observed a gradual reduction in global translation during seed maturation. Transcriptome and translatome profiling revealed specific reduction in the translation of thousands of genes. By including previously published data on germination and seedling establishment, a regulatory network based on polysome occupancy data was constructed: SeedTransNet. Network analysis predicted translational regulatory pathways involving hundreds of genes with distinct functions. The network identified specific transcript sequence features suggesting separate translational regulatory circuits. The network revealed several seed maturation-associated genes as central nodes, and this was confirmed by specific seed phenotypes of the respective mutants. One of the regulators identified, an AWPM19 family protein, PM19-Like1 (PM19L1), was shown to regulate seed dormancy and longevity. This putative RNA-binding protein also affects the translational regulation of its target mRNA, as identified by SeedTransNet. Our data show the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions.

KW - Arabidopsis thaliana

KW - mRNA regulation

KW - ribosome

KW - seed germination

KW - seed maturation

KW - translatome profiling

UR - https://www.scopus.com/pages/publications/85160085758

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DO - 10.1093/jxb/erac394

M3 - Article

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SN - 0022-0957

VL - 74

SP - 2416

EP - 2432

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

IS - 7

ER -

SeedTransNet: A directional translational network revealing regulatory patterns during seed maturation and germination

Abstract

Bibliographical note

Keywords

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