Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo

Abstract

During early plant embryogenesis, precursors for all major tissues and stem cells are formed. While several components of the regulatory framework are known, how cell fates are instructed by genome-wide transcriptional activity remains unanswered - in part because of difficulties in capturing transcriptome changes at cellular resolution. Here, we have adapted a two-component transgenic labelling system to purify cell type-specific nuclear RNA and generate a transcriptome atlas of early Arabidopsis embryo development, with focus on root stem cell niche formation. We validated the dataset through gene expression analysis, and show that gene activity shifts in a spatio-temporal manner, likely signifying transcriptional reprogramming, to induce developmental processes reflecting cell states and state transitions. This atlas provides the most comprehensive tissue- and cell-specific description of genome-wide gene activity in the early plant embryo, and serves as a valuable resource for understanding the genetic control of early plant development.

Initiation and regulation of vascular tissue identity in theArabidopsisembryo

“…At this stage the outer cells acquire protoderm identity (Abe et al, 2003) and we find that the inner cells express multiple vascular marker genes, identifying these cells as the first with vascular attributes. These findings are in line with results of a recent transcriptome study which found that the transcriptome of these (inner) cells is similar to that of the later vascular cells (Palovaara et al, 2017). No ground tissue markers have so far been found to be present in the inner lower tier cells (unpublished).…”

“…The route to a vascular-specific expression pattern starts in the 16-cell stage embryo rather than at early globular stage as previous reports have suggested. In previous work, inner lower tier cells at 16-cell stage were shown to resemble their vascular daughter cells at the globular stage using GO term enrichment in transcriptomes (Palovaara et al, 2017) . Indeed, we find that many vascular marker genes start expression at 16-cell stage, where they are exclusively expressed in the inner cells: DOF6, IQD15, PEAR1, SOK1, WOL and ZLL ( Figure 1A).…”

“…Vascular-enriched genes were selected based on their expression in the early vascular cells, using a cell-type specific embryo transcriptome atlas (Palovaara et al, 2017) and additional publicly available vascular-specific transcriptome datasets ( Figure 2A) (Brady et al, 2007;Belmonte et al, 2013;Kondo et al, 2015;Melnyk et al, 2018).…”

“…The early embryo is an attractive model given that it lacks confounding wound response or extensive proliferation. Its simplicity and predictable division pattern allows detection of early developmental defects (Scheres et al, 1994) and available transcriptome resources (Palovaara et al, 2017;Belmonte et al, 2013;Schon and Nodine, 2017;Slane et al, 2014) enables in-depth investigations of vascular identity establishment.…”

A shared cis-regulatory module activates transcription in the suspensor of plant embryos

“…Whereas the embryo proper undergoes many developmental and morphological changes to eventually become the mature embryo within the seed, the suspensor is a terminally differentiated embryo region that degenerates as the embryo matures. Several studies have shown that different genes are expressed in the embryo proper and suspensor (4)(5)(6)(7)(8), but how these genes are organized into regulatory networks (9) operating in the different embryo regions remains unknown.…”