Developmental and genomic architecture of plant embryogenesis: from model plant to crops

Abstract

Embryonic development represents an important reproductive phase of sexually reproducing plant species. The fusion of egg and sperm produces the plant zygote, a totipotent cell that, through cell division and cell identity specification in early embryogenesis, establishes the major cell lineages and tissues of the adult plant. The subsequent morphogenesis phase produces the full-sized embryo, while the late embryogenesis maturation process prepares the seed for dormancy and subsequent germination, ensuring continuation of the plant life cycle. In this review on embryogenesis, we compare the model eudicot Arabidopsis thaliana with monocot crops, focusing on genome activation, paternal and maternal regulation of early zygote development, and key organizers of patterning, such as auxin and WOX transcription factors. While the early stages of embryo development are apparently conserved among plant species, embryo maturation programs have diversified between eudicots and monocots. This diversification in crop species reflects the likely effects of domestication on seed quality traits that are determined during embryo maturation, and also assures seed germination in different environmental conditions. This review describes the most important features of embryonic development in plants, and the scope and applications of genomics in plant embryo studies.

Keywords: embryo patterning; embryogenesis; genomics; transcription factors; transcriptomics; zygote genome activation.

Figure 1

Embryo development in dicot Arabidopsis and monocot Graminae. (A)Arabidopsis embryo development from zygote to mature stages, showing cell identity markers WOX2 (blue), WOX8 (yellow), WOX5 (purple), and the auxin transporter PIN1 (orange lines). (B) Gramineous embryo development from zygote to the mature developmental stage. WOX2 and WOX8 are expressed in zygotes of rice (Anderson et al., 2017) and maize (Chen et al., 2017), but in situ assays have shown that ZmWOX2A and ZmWOX5 expression occurs later. ZmPIN1 (orange) is first expressed at 6 DAP in maize. Shoot apical meristem (SAM), root apical meristem (RAM), suspensor (Su), coleoptile (Cp), scutellum (Sc), epiblast (Ep), and coleorhiza (Cr), based on Souèges (1924), Van Lammeren (1986), Itoh et al. (2005), and Xiang et al. (2019).

Figure 2

Main processes during embryonic development. The activation of the zygotic genome in early phases involves several genetic processes described in blue, while in red are the processes that participate in the formation of the embryo pattern setting and specification of the primary plant tissues. The maturation processes are highlighted in green and include the last steps of embryonic development.