A multiplexed transcriptomic analysis of a plant embryonic hourglass

The embryo defines the primordial developmental stage of multicellular organisms, from fertilization of the zygote to the formation of tissue layers and organs. Animal zoologists ^{1, 2, 3} described a period of maximum morphological similarity between embryos of different species within related taxa, later termed the phylotypic stage ⁴ of mid-embryogenesis. Modern transcriptomic studies identified a phylotypic pattern of gene expression in Drosophila, zebrafish, and the flowering plant Arabidopsis, featuring enhanced accumulation of evolutionarily older and conserved transcripts during mid-embryogenesis ^{5, 6, 7} . Such plots of transcriptomic age and divergence conform to the “hourglass models” of morphological similarities described by 19 ^th century embryologists. Chronological descriptions of the phylotypic stage are problematic for plants, where embryogenesis extends throughout the life cycle and the mid-point of seed maturation is morphologically and chronologically variable among taxa ⁷ . Here we use multiplexed spatial-transcriptomic analyses to investigate the homology of the grass embryo, which evolved ∼ 150 million years since the divergence of eudicots and grasses ⁸ . Our data support a model where the single maize embryonic leaf (cotyledon) is a novel, bi-partite organ derived within the monocotyledonous grasses, after the evolution of the ancestral angiosperm cotyledon from a modified embryonic leaf ^{9, 10} . We describe a maize embryonic-organ-initiation genetic-network that uses ancient and conserved genes, comprising a phylotypic pattern of “mid embryogenesis” during the ancestrally conserved initiation of histogenesis and organogenic growth in plant and animal embryos.