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Under adverse conditions such as shade or elevated temperatures, cotyledon expansion is reduced and hypocotyl growth is promoted to optimize plant architecture. The mechanisms underlying the repression of cotyledon cell expansion remain unknown. Here, we report that the nuclear abundance of the BES1 transcription factor decreased in the cotyledons and increased in the hypocotyl in Arabidopsis thaliana under shade or warmth. Brassinosteroid levels did not follow the same trend. PIF4 and COP1 increased their nuclear abundance in both organs under shade or warmth. PIF4 directly bound the BES1 promoter to enhance its activity but indirectly reduced BES1 expression. COP1 physically interacted with the BES1 protein, promoting its proteasome degradation in the cotyledons. COP1 had the opposite effect in the hypocotyl, demonstrating organ-specific regulatory networks. Our work indicates that shade or warmth reduces BES1 activity by transcriptional and post-translational regulation to inhibit cotyledon cell expansion.

Brassinosteroids (BRs) play essential roles in growth and development in seed plants;1 disturbances in BR homeostasis lead to altered mitotic activity in meristems2,3 and organ boundaries4,5 and to changes in meristem determinacy.6 An intricate signaling cascade linking the perception of BRs at the plasma membrane to the regulation of master transcriptional regulators belonging to the BEH, for BES1 homologues, family7 has been described in great detail in model angiosperms. Homologs of these transcription factors are present in streptophyte algae and in land plant lineages where BR signaling or function is absent or has not yet been characterized. The genome of the bryophyte Marchantia polymorpha does not encode for BR receptors but includes one close ortholog of Arabidopsis thaliana BRI1-EMS-SUPPRESSOR 1 (AtBES1)8 and Arabidopsis thaliana BRASSINAZOLE-RESISTANT 1 (AtBZR1),9 MpBES1. Altered levels of MpBES1 severely compromised cell division and differentiation, resulting in stunted thalli that failed to differentiate adult tissues and reproductive organs. The transcriptome of Mpbes1 knockout plants revealed a significant overlap with homologous functions controlled by AtBES1 and AtBZR1, suggesting that members of this gene family share a subset of common targets. Indeed, MpBES1 behaved as a gain-of-function substitute of AtBES1/AtBZR1 when expressed in Arabidopsis, probably because it mediates conserved functions but evades the regulatory mechanisms that native counterparts are subject to. Our results show that this family of transcription factors plays an ancestral role in the control of cell division and differentiation in plants and that BR signaling likely co-opted this function and imposed additional regulatory checkpoints upon it.

Light signaling pathways interact with the circadian clock to help organisms synchronize physiological and developmental processes to periodic environmental cycles. The plant photoreceptors responsible for clock resetting have been characterized, but signaling components that link the photoreceptors to the clock remain to be identified. Members of the family of NIGHT LIGHT–INDUCIBLE AND CLOCK-REGULATED (LNK) genes play key roles linking light regulation of gene expression to the control of daily and seasonal rhythms in Arabidopsis thaliana. Particularly, LNK1 and LNK2 were shown to control circadian rhythms, photomorphogenic responses, and photoperiod-dependent flowering time. Here we analyze the role of the four members of the LNK family in Arabidopsis in these processes. We found that depletion of the closely related LNK3 and LNK4 in a lnk1;lnk2 mutant background affects circadian rhythms, but not other clock-regulated processes such as flowering time and seedling photomorphogenesis. Nevertheless, plants defective in all LNK genes (lnkQ quadruple mutants) display developmental alterations that lead to increased rosette size, biomass, and enhanced phototropic responses. Our work indicates that members of the LNK family have both distinctive and partially overlapping functions, and are an essential link to orchestrate light-regulated developmental processes.