Somatic embryo initiation by rice BABY BOOM1 involves activation of zygote‐expressed auxin biosynthesis genes

Abstract

Summary Plant embryogenesis results from the fusion of male and female gametes but can also be induced in somatic cells. The molecular pathways for embryo initiation are poorly understood, especially in monocots. In rice, the male gamete expressed BABY BOOM1 (OsBBM1) transcription factor functions as an embryogenic trigger in the zygote and can also promote somatic embryogenesis when ectopically expressed in somatic tissues. We used gene editing, transcriptome profiling, and chromatin immunoprecipitation to determine the molecular players involved in embryo initiation downstream of OsBBM1. We identify OsYUCCA (OsYUC) auxin biosynthesis genes as direct targets of OsBBM1. Unexpectedly, these OsYUC targets in zygotes are expressed only from the maternal genome, whereas the paternal genome exclusively provides functional OsBBM1 to initiate embryogenesis. Induction of somatic embryogenesis by exogenous auxin requires OsBBM genes and downstream OsYUC targets. Ectopic OsBBM1 initiates somatic embryogenesis without exogenous auxins but requires functional OsYUC genes. Thus, an OsBBM‐OsYUC module is a key player for both somatic and zygotic embryogenesis in rice. Zygotic embryo initiation involves a partnership of male and female genomes, through which paternal OsBBM1 activates maternal OsYUC genes. In somatic embryogenesis, exogenous auxin triggers OsBBM1 expression, which then activates endogenous auxin biosynthesis OsYUC genes.

Identification of a novel and plant height-independent QTL for coleoptile length in barley and validation of its effect using near isogenic lines

“…Subsequently, three genes emerge as primary targets within this interval. One of the genes, HORVU.MOREX.r3.5HG0481610 is orthologous to OsYUC9 in rice, which is involved in auxin biosynthesis (Khanday et al 2023 ; Kim et al 2023 ). Auxins can modify plant cell walls and are crucial for coleoptile cell elongation and expansion (Philippar et al 1999 ; Catalá et al 2000 ).…”

RWP-RK Domain 3 (OsRKD3) induces somatic embryogenesis in black rice

“…Ectopic overexpression of rice BBM1 (OsBBM1) can induce somatic embryogenesis on rice leaves even in the absence of auxin [ 44 ]. It is possible that OsBBM1 induces the initiation of somatic embryos in rice by promoting the activation of OsYUCCA (OsYUC) genes, which are known to be involved in the biosynthesis of auxin [ 55 ]. It is possible that the expression of BBM genes in our experiments is below the level of detection and/or that these genes are regulated through a different transcriptional pathway.…”

Multifaceted roles of transcription factors during plant embryogenesis

“…Elevated expression of BBM-like PLT gene members, such as PLT1, PLT2, PLT3, and PLT7, has been demonstrated to induce somatic embryogenesis. Notably, PLT1 and PLT3 were found to recover early-stage embryo defects of plt2 bbm mutants, suggesting a redundant and overlapping role of BBM and BBM-like genes in Boutilier et al, 2002;Srinivasan et al, 2007;Deng et al, 2009;Heidmann et al, 2011;Florez et al, 2015;Mookkan et al, 2017;Mookkan et al, 2017;Yavuz et al, 2020;Nelson-Vasilchik et al, 2022;Qi et al, 2022;Khanday et al, 2023;Xiao et al, 2023, Chen et…”

“…An OsBBM1 - OsYUC module has been shown to play an important role in both zygotic embryogenesis and somatic embryogenesis in rice ( Khanday et al., 2023 ). Paternal-genome-originated OsBBM1 directly triggers maternal-genome-originated auxin biosynthesis gene OsYUCCA ( OsYUC ) to initiate zygotic embryo development; while under the culture conditions, exogenous auxin induces OsBBM1 , which then activates endogenous OsYUC genes ( OsYUC6 , OsYUC7 and OsYUC9 ) to promote somatic embryogenesis ( Khanday et al., 2018 ; Khanday et al., 2023 ).…”