Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants

The appearance of plant organs mediated the explosive radiation of land plants, which shaped the biosphere and allowed the establishment of terrestrial animal life. The evolution of organs and immobile gametes required the coordinated acquisition of novel gene functions, the co-option of existing ge...

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Main Authors: Julca, Irene, Ferrari, Camilla, Flores-Tornero, María, Proost, Sebastian, Lindner, Ann-Cathrin, Hackenberg, Dieter, Steinbachová, Lenka, Michaelidis, Christos, Gomes Pereira, Sónia, Misra, Chandra Shekhar, Kawashima, Tomokazu, Borg, Michael, Berger, Frédéric, Goldberg, Jacob, Johnson, Mark, Honys, David, Twell, David, Sprunck, Stefanie, Dresselhaus, Thomas, Becker, Jörg D., Mutwil, Marek
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2022
Subjects:
Online Access:https://hdl.handle.net/10356/157013
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Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-157013
record_format dspace
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Plant Protein
Gene Expression Profiling
spellingShingle Science::Biological sciences
Plant Protein
Gene Expression Profiling
Julca, Irene
Ferrari, Camilla
Flores-Tornero, María
Proost, Sebastian
Lindner, Ann-Cathrin
Hackenberg, Dieter
Steinbachová, Lenka
Michaelidis, Christos
Gomes Pereira, Sónia
Misra, Chandra Shekhar
Kawashima, Tomokazu
Borg, Michael
Berger, Frédéric
Goldberg, Jacob
Johnson, Mark
Honys, David
Twell, David
Sprunck, Stefanie
Dresselhaus, Thomas
Becker, Jörg D.
Mutwil, Marek
Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
description The appearance of plant organs mediated the explosive radiation of land plants, which shaped the biosphere and allowed the establishment of terrestrial animal life. The evolution of organs and immobile gametes required the coordinated acquisition of novel gene functions, the co-option of existing genes and the development of novel regulatory programmes. However, no large-scale analyses of genomic and transcriptomic data have been performed for land plants. To remedy this, we generated gene expression atlases for various organs and gametes of ten plant species comprising bryophytes, vascular plants, gymnosperms and flowering plants. A comparative analysis of the atlases identified hundreds of organ- and gamete-specific orthogroups and revealed that most of the specific transcriptomes are significantly conserved. Interestingly, our results suggest that co-option of existing genes is the main mechanism for evolving new organs. In contrast to female gametes, male gametes showed a high number and conservation of specific genes, which indicates that male reproduction is highly specialized. The expression atlas capturing pollen development revealed numerous transcription factors and kinases essential for pollen biogenesis and function.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Julca, Irene
Ferrari, Camilla
Flores-Tornero, María
Proost, Sebastian
Lindner, Ann-Cathrin
Hackenberg, Dieter
Steinbachová, Lenka
Michaelidis, Christos
Gomes Pereira, Sónia
Misra, Chandra Shekhar
Kawashima, Tomokazu
Borg, Michael
Berger, Frédéric
Goldberg, Jacob
Johnson, Mark
Honys, David
Twell, David
Sprunck, Stefanie
Dresselhaus, Thomas
Becker, Jörg D.
Mutwil, Marek
format Article
author Julca, Irene
Ferrari, Camilla
Flores-Tornero, María
Proost, Sebastian
Lindner, Ann-Cathrin
Hackenberg, Dieter
Steinbachová, Lenka
Michaelidis, Christos
Gomes Pereira, Sónia
Misra, Chandra Shekhar
Kawashima, Tomokazu
Borg, Michael
Berger, Frédéric
Goldberg, Jacob
Johnson, Mark
Honys, David
Twell, David
Sprunck, Stefanie
Dresselhaus, Thomas
Becker, Jörg D.
Mutwil, Marek
author_sort Julca, Irene
title Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
title_short Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
title_full Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
title_fullStr Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
title_full_unstemmed Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
title_sort comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
publishDate 2022
url https://hdl.handle.net/10356/157013
_version_ 1759852997907578880
spelling sg-ntu-dr.10356-1570132023-02-28T17:12:01Z Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants Julca, Irene Ferrari, Camilla Flores-Tornero, María Proost, Sebastian Lindner, Ann-Cathrin Hackenberg, Dieter Steinbachová, Lenka Michaelidis, Christos Gomes Pereira, Sónia Misra, Chandra Shekhar Kawashima, Tomokazu Borg, Michael Berger, Frédéric Goldberg, Jacob Johnson, Mark Honys, David Twell, David Sprunck, Stefanie Dresselhaus, Thomas Becker, Jörg D. Mutwil, Marek School of Biological Sciences Science::Biological sciences Plant Protein Gene Expression Profiling The appearance of plant organs mediated the explosive radiation of land plants, which shaped the biosphere and allowed the establishment of terrestrial animal life. The evolution of organs and immobile gametes required the coordinated acquisition of novel gene functions, the co-option of existing genes and the development of novel regulatory programmes. However, no large-scale analyses of genomic and transcriptomic data have been performed for land plants. To remedy this, we generated gene expression atlases for various organs and gametes of ten plant species comprising bryophytes, vascular plants, gymnosperms and flowering plants. A comparative analysis of the atlases identified hundreds of organ- and gamete-specific orthogroups and revealed that most of the specific transcriptomes are significantly conserved. Interestingly, our results suggest that co-option of existing genes is the main mechanism for evolving new organs. In contrast to female gametes, male gametes showed a high number and conservation of specific genes, which indicates that male reproduction is highly specialized. The expression atlas capturing pollen development revealed numerous transcription factors and kinases essential for pollen biogenesis and function. Ministry of Education (MOE) Nanyang Technological University Submitted/Accepted version I.J. is supported by Singaporean Ministry of Education grant MOE2018-T2-2-053, while M.M. is supported by a NTU Start-Up Grant. ERA-CAPS EVO-REPRO I2163 and FWF grant P30802 were awarded to F.B.; FCT ERA-CAPS-0001-2014 and PTDC-BIA-FBT-28484-2017 to J.D.B.; and ERA-CAPS EVO-REPRO DR 334/12-1 to S.S. and T.D. D. Hackenberg was supported by ERA-CAPS UK Biotechnology and Biological Research Council grant BB/N005090 awarded to D.T.; M.B. was supported through the FWF Lise Meitner fellowship M1818. The Vienna BioCenter Core Facilities GmbH (VBCF) Plant Sciences Facility acknowledges funding from the Austrian Federal Ministry of Education, Science and Research and the City of Vienna. L.S. was supported by CSF grant 17-23183S. C.M. and D. Honys were supported by the Czech Ministry of Education, Youth and Sport (LTC18034 and LTAIN19030) through the European Regional Development Fund-Project “Centre for Experimental Plant Biology” number CZ.02.1.01/0.0/0.0/16_019/0000738. The Genomics Unit of Instituto Gulbenkian de Ciência was partially supported by the ONEIDA Project (LISBOA01-0145-FEDER-016417) co-funded by FEEI–‘Fundos Europeus Estruturais e de Investimento’ from the ‘Programa Operacional Regional Lisboa 2020’ and by national funds from FCT–‘Fundação para a Ciência e a Tecnologia’. C.S.M. acknowledges a doctoral fellowship from the FCT (PD/BD/114362/2016) under the Plants for Life PhD Program. J.D.B. received salary support from the FCT through an ‘Investigador FCT’ position. M.J. and J.G. were supported by a US National Science Foundation grant (IOS1540019). 2022-04-29T06:51:49Z 2022-04-29T06:51:49Z 2021 Journal Article Julca, I., Ferrari, C., Flores-Tornero, M., Proost, S., Lindner, A., Hackenberg, D., Steinbachová, L., Michaelidis, C., Gomes Pereira, S., Misra, C. S., Kawashima, T., Borg, M., Berger, F., Goldberg, J., Johnson, M., Honys, D., Twell, D., Sprunck, S., Dresselhaus, T., ...Mutwil, M. (2021). Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants. Nature Plants, 7(8), 1143-1159. https://dx.doi.org/10.1038/s41477-021-00958-2 2055-026X https://hdl.handle.net/10356/157013 10.1038/s41477-021-00958-2 34253868 2-s2.0-85110533979 8 7 1143 1159 en MOE2018-T2-2-053 Nature Plants © 2021 The Author(s), under exclusive licence to Springer Nature Limited. All rights reserved. This paper was published in Nature Plants and is made available with permission of The Author(s). application/pdf