Comparative analysis of embryo proper and suspensor transcriptomes in plant embryos with different morphologies

Abstract

An important question is what genes govern the differentiation of plant embryos into suspensor and embryo proper regions following fertilization and division of the zygote. We compared embryo proper and suspensor transcriptomes of four plants that vary in embryo morphology within the suspensor region. We determined that genes encoding enzymes in several metabolic pathways leading to the formation of hormones, such as gibberellic acid, and other metabolites are up-regulated in giant scarlet runner bean and common bean suspensors. Genes involved in transport and Golgi body organization are up-regulated within the suspensors of these plants as well, strengthening the view that giant specialized suspensors serve as a hormone factory and a conduit for transferring substances to the developing embryo proper. By contrast, genes controlling transcriptional regulation, development, and cell division are up-regulated primarily within the embryo proper. Transcriptomes from less specialized soybean and Arabidopsis suspensors demonstrated that fewer genes encoding metabolic enzymes and hormones are up-regulated. Genes active in the embryo proper, however, are functionally similar to those active in scarlet runner bean and common bean embryo proper regions. We uncovered a set of suspensor- and embryo proper–specific transcription factors (TFs) that are shared by all embryos irrespective of morphology, suggesting that they are involved in early differentiation processes common to all plants. Chromatin immunoprecipitation sequencing (ChIP-Seq) experiments with scarlet runner bean and soybean WOX9, an up-regulated suspensor TF, gained entry into a regulatory network important for suspensor development irrespective of morphology.

Gene expression variation in Arabidopsis embryos at single-nucleus resolution

“…Altogether, these results suggested that genes preferentially expressed in ACL clusters, and especially the vas and div clusters are under stronger purifying selection compared to those in BCL clusters, especially the col cluster, which are mutating at a faster rate. This is also consistent with the more variable morphologies of suspensors relative to embryo propers (Chen et al, 2021).…”

“…This allowed us to construct a gene expression atlas of Arabidopsis embryos at the globular stage when the basic body plan is being established. Our results build upon foundational research examining the divergence of gene expression between the first two sporophytic cell lineages ( Belmonte et al, 2013 ; Chen et al, 2021 ; Zhou et al, 2020 ) to help characterize how distinct gene expression programs, and corresponding cell types, are generated during early embryogenesis. Because evolutionary trajectories and transcripts encoding epigenetic factors or transcriptional regulators varied across early embryonic cell types, we surveyed these aspects to gain insights into how distinct gene expression programs are established in early embryos.…”

“…However, these transcriptomes were generated from whole embryos. Additional studies have revealed genes that are preferentially expressed in broad ( Belmonte et al, 2013 ; Casson et al, 2005 ; Chen et al, 2021 ; Slane et al, 2014 ; Zhou et al, 2020 ) or more specific ( Palovaara et al, 2017 ) regions of plant embryos, but either lack cellular resolution or were contaminated with RNAs derived from the maternal seed coat that encompasses the developing embryo ( Schon and Nodine, 2017 ).…”

Methods forin situquantitative root biology

“…Module I was aimed for nuclei and chromatin analysis, and might be used to build chromatin accessibility maps when combined with ATAC-seq and laser-capture microdissection (Chen et al 2021). This module also allows studying cell differentiation status, as chromatin organization is tightly linked to gene expression regulation and to the differentiation status of the cell.…”

Endosperm evolution by duplicated and neofunctionalized Type I MADS-box transcription factors

“…The expression data of Type I MADS-box genes in A. thaliana were extracted from Klepicova et al ( 2016) for a spectrum of different organ types and developmental stages and Belmonte et al (2013) for specific compartments in developing seeds. The other transcriptomes used in this study were retrieved from maize (Chen et al 2014;Walley et al 2016), rice (Paul et al 2020), soybean (Chen et al 2021), castor bean (Xu et al 2014), tomato (Pattison et al 2015), coconut (Saensuk et al 2016), avocado (Ge et al 2019), monkeyflower (Flores-Vergara et al 2019), coffee (Ivamoto et al 2017), Nymphaea thermarum (Povilus and Friedman 2021), Picea (Nystedt et al 2013), and Gnetum (Hou et al 2019;Deng et al 2020). Gene identifiers in Supplementary Table…”