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Histone Demethylases Coordinate the Antagonistic Interaction Between Abscisic Acid and Brassinosteroid Signaling in Arabidopsis.

ABSTRACT: Abscisic acid (ABA) interacts antagonistically with brassinosteroids (BRs) to control plant growth and development in response to stress. The response to environmental cues includes hormonal control via epigenetic regulation of gene expression. However, the details of the ABA-BR crosstalk remain largely unknown. Here, we show that JUMONJI-C domain containing histone demethylases (JMJs) coordinate the antagonistic interaction between ABA and BR signaling pathways during the post-germination stage in Arabidopsis. BR blocks ABA-mediated seedling arrest through repression of JMJ30. JMJs remove the repressive histone marks from the BRASSINAZOLE RESISTANT1 (BZR1) locus for its activation to balance ABA and BR signaling pathways. JMJs and BZR1 co-regulate genes encoding three membrane proteins, a regulator of vacuole morphology, and two lipid-transfer proteins, each of which play a different role in transport. BZR1 also regulates stimuli-related target genes in a JMJ-independent pathway. Our findings suggest that the histone demethylases integrate ABA and BR signals, leading to changes in growth program after germination.

SUBMITTER: Wu J

PROVIDER: S-EPMC7724051 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Histone Demethylases Coordinate the Antagonistic Interaction Between Abscisic Acid and Brassinosteroid Signaling in <i>Arabidopsis</i>.

Wu Jinfeng J Yan Mingli M Zhang Dawei D Zhou Dinggang D Yamaguchi Nobutoshi N Ito Toshiro T

Frontiers in plant science 20201125

Abscisic acid (ABA) interacts antagonistically with brassinosteroids (BRs) to control plant growth and development in response to stress. The response to environmental cues includes hormonal control via epigenetic regulation of gene expression. However, the details of the ABA-BR crosstalk remain largely unknown. Here, we show that JUMONJI-C domain containing histone demethylases (JMJs) coordinate the antagonistic interaction between ABA and BR signaling pathways during the post-germination stage ...[more]

PMID: 33324437

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Project description:BackgroundBrassinosteroids (BRs) play crucial roles in plant development and also promote tolerance to a range of abiotic stresses. Although much has been learned about their roles in plant development, the mechanisms by which BRs control plant stress responses and regulate stress-responsive gene expression are not fully known. Since BR interacts with other plant hormones, it is likely that the stress tolerance conferring ability of BR lies in part in its interactions with other stress hormones.ResultsUsing a collection of Arabidopsis mutants that are either deficient in or insensitive to abscisic acid (ABA), ethylene (ET), jasmonic acid (JA) and salicylic acid (SA), we studied the effects of 24-epibrassinloide (EBR) on basic thermotolerance and salt tolerance of these mutants. The positive impact of EBR on thermotolerance in proportion to wild type was evident in all mutants studied, with the exception of the SA-insensitive npr1-1 mutant. EBR could rescue the ET-insensitive ein2 mutant from its hypersensitivity to salt stress-induced inhibition of seed germination, but remained ineffective in increasing the survival of eto1-1 (ET-overproducer) and npr1-1 seedlings on salt. The positive effect of EBR was significantly greater in the ABA-deficient aba1-1 mutant as compared to wild type, indicating that ABA masks BR effects in plant stress responses. Treatment with EBR increased expression of various hormone marker genes in both wild type and mutant seedlings, although to different levels.ConclusionsThese results together indicate that the redox-sensitive protein NPR1 (NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1), a master regulator of SA-mediated defense genes, is likely a critical component of EBR-mediated increase in thermotolerance and salt tolerance, but it is not required for EBR-mediated induction of PR-1 (PATHOGENESIS-RELATED1) gene expression; that BR exerts anti-stress effects independently as well as through interactions with other hormones; that ABA inhibits BR effects during stress; and that BR shares transcriptional targets with other hormones.

Project description:Leaf senescence is induced by various internal and external stimuli. Dark-induced senescence has been extensively investigated, but the detailed mechanism underlying it is not well understood. The red light/far-red light receptor phytochrome B and its downstream transcription factors, PYHTOCHROME INTERACTING FACTORs (PIFs) 4 and 5, are known to play an important role in dark-induced senescence. Furthermore, the senescence-inducing phytohormones, ethylene and abscisic acid (ABA) are reported to be involved in dark-induced senescence. In this study, we analyzed the relationship between ethylene, ABA and PIFs in dark-induced leaf senescence. A triple mutant of the core ABA signaling components; SNF1-related protein kinases 2D (SRK2D), SRK2E, and SRK2I, displayed an ABA insensitive phenotype in ABA-induced senescence, whilst the ethylene insensitive mutant ein2 demonstrated low sensitivity to ABA, suggesting that ethylene signaling is involved in ABA-induced senescence. However, the pif4 pif5 mutant did not display low sensitivity to ABA, suggesting that PIF4 and PIF5 act upstream of ABA signaling. Although PIF4 and PIF5 reportedly regulate ethylene production, the triple mutant ein2 pif4 pif5 showed a stronger delayed senescence phenotype than ein2 or pif4 pif5, suggesting that EIN2 and PIF4/PIF5 partially regulate leaf senescence independently of each other. While direct target genes for PIF4 and PIF5, such as LONG HYPOCOTYL IN FAR-RED1 (HFR1) and PHYTOCHROME INTERACTING FACTOR 3-LIKE 1 (PIL1), showed transient upregulation under dark conditions (as is seen in the shade avoidance response), expression of STAY GREEN1 (SGR1), ORESARA1 (ORE1) and other direct target genes of PIF5, continued to increase during dark incubation. It is possible that transcription factors other than PIF4 and PIF5 are involved in the upregulation of SGR1 and ORE1 at a later stage of dark-induced senescence. Possible candidates are senescence-induced senescence regulators (SIRs), which include the NAC transcription factors ORE1 and AtNAP. In fact, ORE1 is known to bind to the SGR1 promoter and promotes its expression. It is therefore inferred that the phytochrome-PIF pathway regulates initial activation of senescence and subsequently, induced SIRs reinforce leaf senescence during dark-induced senescence.

Dataset Information

Histone Demethylases Coordinate the Antagonistic Interaction Between Abscisic Acid and Brassinosteroid Signaling in Arabidopsis.

Publications

Histone Demethylases Coordinate the Antagonistic Interaction Between Abscisic Acid and Brassinosteroid Signaling in <i>Arabidopsis</i>.

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