Brassinosteroids repress the seed maturation program during the seed-to-seedling transition

Abstract

In flowering plants, repression of the seed maturation program is essential for the transition from the seed to the vegetative phase, but the underlying mechanisms remain poorly understood. The B3-domain protein VIVIPAROUS1/ABSCISIC ACID INSENSITIVE3-LIKE 1 (VAL1) is involved in repressing the seed maturation program. Here we uncovered a molecular network triggered by the plant hormone brassinosteroid (BR) that inhibits the seed maturation program during the seed-to-seedling transition in Arabidopsis (Arabidopsis thaliana). val1-2 mutant seedlings treated with a BR biosynthesis inhibitor form embryonic structures, whereas BR signaling gain-of-function mutations rescue the embryonic structure trait. Furthermore, the BR-activated transcription factors BRI1-EMS-SUPPRESSOR 1 (BES1) and BRASSINAZOLE-RESISTANT 1 (BZR1) bind directly to the promoter of AGAMOUS-LIKE15 (AGL15), which encodes a transcription factor involved in activating the seed maturation program, and suppress its expression. Genetic analysis indicated that BR signaling is epistatic to AGL15 and represses the seed maturation program by downregulating AGL15. Finally, we showed that the BR-mediated pathway functions synergistically with the VAL1/2-mediated pathway to ensure the full repression of the seed maturation program. Together, our work uncovered a mechanism underlying the suppression of the seed maturation program, shedding light on how BR promotes seedling growth.

Dynamics of Protein Phosphorylation during Arabidopsis Seed Germination

“…BSK1 is phosphorylated at S230 by the BR receptor BRI1, thereby activating BR responses [66]. BR are positive regulators of seed germination and have recently been ascribed a major function in seed-to-seedling transition [67]. Moreover, bsk5 seeds exhibit delayed germination and a higher sensitivity towards ABA [68].…”

AGL15 Promotion of Somatic Embryogenesis: Role and Molecular Mechanism

“…Interestingly, Ruan et al ( 2021 ) also show that wild type seedlings treated with BR biosynthesis inhibitors have darker green, downward curling leaves that look similar to seedings overexpressing AGL15 (Fernandez et al, 2000 ). AGL15 binds to the promoter regions of BZR1 and BES1 ( Supplementary Figure 1 ) and at least for BZR1 , represses transcript accumulation.…”

“…While Brassinosteroids (BR) have been reported to enhance SE (at least in combination with cytokinin: CK—Chone et al, 2018 ), a recent publication reports on direct interactions between AGL15, BR signaling, and SE (Ruan et al, 2021 ). This paper documents experiments showing that BR promotes the embryo to seedling transition, at least in part through repression of AGL15 expression.…”

“…AGL15 is involved in the production of the SEs as shown by double and triple mutants with an agl15 loss-of-function mutant. Ruan et al ( 2021 ) hypothesized that BES1 and BZR1 may also directly regulate GA biosynthetic genes, increasing bioactive GA levels and thereby removing negative interaction of BES1/BZR1 by the DELLA proteins.…”

A reevaluation of the role of the ASIL trihelix transcription factors as repressors of the seed maturation program

“…These proteins indirectly repress the SSP genes, LEC1 , LEC2 , and FUS3 , by recruiting the histone deacetylase HDA19 and PcG proteins and preventing the expression of the activator AGAMOUS‐LIKE15 ( AGL15 ) (Chen et al, 2018 ; Chhun et al, 2016 ; Gao et al, 2009 ; Jia et al, 2013 ; Suzuki et al, 2007 ; Tsukagoshi et al, 2007 ; Yang et al, 2013 ; Zhou et al, 2013 ). The brassinosteroid signaling pathway acts together with VAL1 to repress of AGL15 (Ruan et al, 2021 ). Another repressive transcription factor is SCARECROW‐LIKE15 (SCL15), which acts through its interaction with the histone deacetylase HDA19 (Gao et al, 2015 ).…”