Multiplexed transcriptomic analyzes of the plant embryonic hourglass

Abstract Zoologists have adduced morphological convergence among embryonic stages of closely related taxa, which has been called the phylotypic stage of embryogenesis. Transcriptomic analyzes reveal an hourglass pattern of gene expression during plant and animal embryogenesis, characterized by the a...

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Main Authors: Hao Wu, Ruqiang Zhang, Karl J. Niklas, Michael J. Scanlon
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55803-9
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author Hao Wu
Ruqiang Zhang
Karl J. Niklas
Michael J. Scanlon
author_facet Hao Wu
Ruqiang Zhang
Karl J. Niklas
Michael J. Scanlon
author_sort Hao Wu
collection DOAJ
description Abstract Zoologists have adduced morphological convergence among embryonic stages of closely related taxa, which has been called the phylotypic stage of embryogenesis. Transcriptomic analyzes reveal an hourglass pattern of gene expression during plant and animal embryogenesis, characterized by the accumulation of evolutionarily older and conserved transcripts during mid-embryogenesis, whereas younger less-conserved transcripts predominate at earlier and later embryonic stages. In contrast, comparisons of embryonic gene expression among different animal phyla describe an inverse hourglass pattern, where expression is correlated during early and late stages but not during mid-embryo development. Here, multiplexed spatial-transcriptomic analyzes is used to investigate embryogenesis and homology in maize, which has grass-specific morphology. A set of shared, co-expressed genes is identified during initiation of maize embryonic organs, replete for ancient/conserved genes manifesting an hourglass pattern during mid-embryogenesis. Transcriptomic comparisons of maize and Arabidopsis embryogenesis with that of the moss Physcomitrium patens identify an inverse hourglass pattern across plant phyla, as in animals. The data suggest that the phylotypic stages in plants and animals are characterized by expression of ancient and conserved genes during histogenesis, organization of embryonic axes, and initial morphogenesis. We propose a mechanism for gene evolution during the innovation of morphological novelty.
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spelling doaj-art-b5d929955a1e47d4b45ada23f5030c472025-01-19T12:32:13ZengNature PortfolioNature Communications2041-17232025-01-0116111610.1038/s41467-024-55803-9Multiplexed transcriptomic analyzes of the plant embryonic hourglassHao Wu0Ruqiang Zhang1Karl J. Niklas2Michael J. Scanlon3School of Integrative Plant Science, Plant Biology Section, Cornell UniversitySchool of Integrative Plant Science, Plant Biology Section, Cornell UniversitySchool of Integrative Plant Science, Plant Biology Section, Cornell UniversitySchool of Integrative Plant Science, Plant Biology Section, Cornell UniversityAbstract Zoologists have adduced morphological convergence among embryonic stages of closely related taxa, which has been called the phylotypic stage of embryogenesis. Transcriptomic analyzes reveal an hourglass pattern of gene expression during plant and animal embryogenesis, characterized by the accumulation of evolutionarily older and conserved transcripts during mid-embryogenesis, whereas younger less-conserved transcripts predominate at earlier and later embryonic stages. In contrast, comparisons of embryonic gene expression among different animal phyla describe an inverse hourglass pattern, where expression is correlated during early and late stages but not during mid-embryo development. Here, multiplexed spatial-transcriptomic analyzes is used to investigate embryogenesis and homology in maize, which has grass-specific morphology. A set of shared, co-expressed genes is identified during initiation of maize embryonic organs, replete for ancient/conserved genes manifesting an hourglass pattern during mid-embryogenesis. Transcriptomic comparisons of maize and Arabidopsis embryogenesis with that of the moss Physcomitrium patens identify an inverse hourglass pattern across plant phyla, as in animals. The data suggest that the phylotypic stages in plants and animals are characterized by expression of ancient and conserved genes during histogenesis, organization of embryonic axes, and initial morphogenesis. We propose a mechanism for gene evolution during the innovation of morphological novelty.https://doi.org/10.1038/s41467-024-55803-9
spellingShingle Hao Wu
Ruqiang Zhang
Karl J. Niklas
Michael J. Scanlon
Multiplexed transcriptomic analyzes of the plant embryonic hourglass
Nature Communications
title Multiplexed transcriptomic analyzes of the plant embryonic hourglass
title_full Multiplexed transcriptomic analyzes of the plant embryonic hourglass
title_fullStr Multiplexed transcriptomic analyzes of the plant embryonic hourglass
title_full_unstemmed Multiplexed transcriptomic analyzes of the plant embryonic hourglass
title_short Multiplexed transcriptomic analyzes of the plant embryonic hourglass
title_sort multiplexed transcriptomic analyzes of the plant embryonic hourglass
url https://doi.org/10.1038/s41467-024-55803-9
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AT karljniklas multiplexedtranscriptomicanalyzesoftheplantembryonichourglass
AT michaeljscanlon multiplexedtranscriptomicanalyzesoftheplantembryonichourglass