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

Abstract

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.

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Fig. 1: Expression atlases for seven land plant species.
Fig. 2: Comparison of organ-specific transcriptomes.
Fig. 3: Genomic analysis of the organ specificity of orthogroups.
Fig. 4: Evolutionary analysis of organs.
Fig. 5: Comparison of male development across species.
Fig. 6: A network analysis of male clusters.
Fig. 7: Features of the EVOREPRO database.

Data availability

The fastq files are available for Arabidopsis (E-MTAB-9456), Amborella (E-MTAB-9190), Marchantia (E-MTAB-9457), Physcomitrium (E-MTAB-9466), maize (E-MTAB-9692) and tomato (E-MTAB-9725). The data can be obtained from https://www.ebi.ac.uk/ena.

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Acknowledgements

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 (LISBOA-01-0145-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 (IOS-1540019). Help with sample generation was provided by L. Z. Drábková and D. Reňák. Marchantia growth was performed by the Plant Sciences Facility at the Vienna BioCenter Core Facilities GmbH (VBCF), member of the Vienna BioCenter (VBC), Austria. M. Weigend, C. Löhne and B. Reinken (Botanical Garden of the University of Bonn, Germany) are acknowledged for providing A. trichopoda plant material. D. Shivhare is acknowledged for a preliminary analysis of Physcomitrium RNA-seq data. We thank D. Maizels (http://www.scientific-art.com/) for the illustrations in Figs. 1 and 5.

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J.D.B. and M.M. conceived and designed the analysis. A.-C.L., M.F.-T., S.G.P., C.S.M., J.G., M.J., I.J., L.S., C.M., D. Honys and D. Hackenberg collected the data. F.B., M.B., S.S., T.D., T.K. and D.T. contributed data or analysis tools. I.J., C.F., S.P., A.-C.L. and M.M. performed the analyses. I.J., J.D.B. and M.M. wrote the paper.

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Correspondence to Jörg D. Becker or Marek Mutwil.

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Peer review information Nature Plants thanks Jan de Vries, Dabing Zhang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Julca, I., Ferrari, C., Flores-Tornero, M. et al. Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants. Nat. Plants 7, 1143–1159 (2021). https://doi.org/10.1038/s41477-021-00958-2

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