Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation

Light-regulated developmental processes such as photomorphogenesis and flowering play important roles in the plant life cycle, from seedling emergence to reproduction. Three members of the Arabidopsis thaliana B-BOX DOMAIN PROTEIN (BBX) family, BBX14, BBX15, and BBX16 (hereafter BBX14/15/16), redund...

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Main Authors: Zeeshan Nasim, Nouroz Karim, Hendry Susila, Ji Hoon Ahn
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Current Plant Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S221466282400077X
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author Zeeshan Nasim
Nouroz Karim
Hendry Susila
Ji Hoon Ahn
author_facet Zeeshan Nasim
Nouroz Karim
Hendry Susila
Ji Hoon Ahn
author_sort Zeeshan Nasim
collection DOAJ
description Light-regulated developmental processes such as photomorphogenesis and flowering play important roles in the plant life cycle, from seedling emergence to reproduction. Three members of the Arabidopsis thaliana B-BOX DOMAIN PROTEIN (BBX) family, BBX14, BBX15, and BBX16 (hereafter BBX14/15/16), redundantly regulate flowering time, but whether this genetic redundancy also affects the regulation of photomorphogenesis remains unclear. Here, we show that light induces BBX14/15/16 expression primarily in the hypocotyl, where BBX14/15/16 redundantly repress hypocotyl elongation. PHYTOCHROME-INTERACTING FACTORs (PIFs) negatively regulate BBX14/15/16 expression mainly through GOLDEN-LIKE proteins (GLKs); however, analyses of ChIP-seq data showed that PIFs are recruited to the BBX14/15/16 loci and can also regulate these genes independently of GLKs. ELONGATED HYPOCOTYL 5 (HY5), a major regulator of photomorphogenesis, also directly binds to the BBX14/15/16 loci and regulates their expression. Simultaneous knockdown of BBX14/15/16 resulted in significant downregulation of HY5 and upregulation of PIFs, suggesting that these factors participate in a feedback regulatory loop. Indeed, BBX14/15/16 induced HY5 promoter activity by binding to the HY5 promoter. The brassinosteroid-responsive gene TOUCH4 (TCH4) and several auxin-responsive SMALL AUXIN UPREGULATED RNA (SAUR) genes were upregulated in the BBX14/15/16 knockdown plants, suggesting that auxin and brassinosteroids might participate in BBX14/15/16-mediated hypocotyl regulation. Mutating the predicted BBX-binding sites in SAUR4 and TCH4 impaired their regulation by BBX14/15/16. We propose that BBX14/15/16, together with HY5 and PIFs, form a feedback loop that regulates the expression of auxin- and brassinosteroid-related genes to modulate hypocotyl elongation.
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spelling doaj-art-ff952b48d5b94ac690fe7a4ac1258d552025-08-20T02:50:27ZengElsevierCurrent Plant Biology2214-66282024-12-014010039510.1016/j.cpb.2024.100395Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongationZeeshan Nasim0Nouroz Karim1Hendry Susila2Ji Hoon Ahn3Department of Life Sciences, Korea University, Seoul 02841, South KoreaDepartment of Life Sciences, Korea University, Seoul 02841, South KoreaARC Training Centre for Accelerated Future Crops Development, The Australian National University, Canberra, Australian Capital Territory 6201, AustraliaDepartment of Life Sciences, Korea University, Seoul 02841, South Korea; Corresponding author.Light-regulated developmental processes such as photomorphogenesis and flowering play important roles in the plant life cycle, from seedling emergence to reproduction. Three members of the Arabidopsis thaliana B-BOX DOMAIN PROTEIN (BBX) family, BBX14, BBX15, and BBX16 (hereafter BBX14/15/16), redundantly regulate flowering time, but whether this genetic redundancy also affects the regulation of photomorphogenesis remains unclear. Here, we show that light induces BBX14/15/16 expression primarily in the hypocotyl, where BBX14/15/16 redundantly repress hypocotyl elongation. PHYTOCHROME-INTERACTING FACTORs (PIFs) negatively regulate BBX14/15/16 expression mainly through GOLDEN-LIKE proteins (GLKs); however, analyses of ChIP-seq data showed that PIFs are recruited to the BBX14/15/16 loci and can also regulate these genes independently of GLKs. ELONGATED HYPOCOTYL 5 (HY5), a major regulator of photomorphogenesis, also directly binds to the BBX14/15/16 loci and regulates their expression. Simultaneous knockdown of BBX14/15/16 resulted in significant downregulation of HY5 and upregulation of PIFs, suggesting that these factors participate in a feedback regulatory loop. Indeed, BBX14/15/16 induced HY5 promoter activity by binding to the HY5 promoter. The brassinosteroid-responsive gene TOUCH4 (TCH4) and several auxin-responsive SMALL AUXIN UPREGULATED RNA (SAUR) genes were upregulated in the BBX14/15/16 knockdown plants, suggesting that auxin and brassinosteroids might participate in BBX14/15/16-mediated hypocotyl regulation. Mutating the predicted BBX-binding sites in SAUR4 and TCH4 impaired their regulation by BBX14/15/16. We propose that BBX14/15/16, together with HY5 and PIFs, form a feedback loop that regulates the expression of auxin- and brassinosteroid-related genes to modulate hypocotyl elongation.http://www.sciencedirect.com/science/article/pii/S221466282400077XPhotomorphogenesisPIFsBBXHY5GLKSAURs
spellingShingle Zeeshan Nasim
Nouroz Karim
Hendry Susila
Ji Hoon Ahn
Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
Current Plant Biology
Photomorphogenesis
PIFs
BBX
HY5
GLK
SAURs
title Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
title_full Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
title_fullStr Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
title_full_unstemmed Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
title_short Arabidopsis B-BOX DOMAIN PROTEIN14/15/16 form a feedback loop with ELONGATED HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs to regulate hypocotyl elongation
title_sort arabidopsis b box domain protein14 15 16 form a feedback loop with elongated hypocotyl 5 and phytochrome interacting factors to regulate hypocotyl elongation
topic Photomorphogenesis
PIFs
BBX
HY5
GLK
SAURs
url http://www.sciencedirect.com/science/article/pii/S221466282400077X
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AT hendrysusila arabidopsisbboxdomainprotein141516formafeedbackloopwithelongatedhypocotyl5andphytochromeinteractingfactorstoregulatehypocotylelongation
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