Keunhwa Kim

Gyeongsang National University

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Giltsu Choi

Korea Advanced Institute of Science and Technology

Jinkil Jeong

Korea Advanced Institute of Science and Technology

Gabyong Bae

Korea Advanced Institute of Science and Technology

Jaewook Kim

Pohang University of Science and Technology

Youn‐Il Park

Chungnam National University

Jieun Shin

Konyang University

Kijong Song

Korea Advanced Institute of Science and Technology

Meng Chen

Hunan Agricultural University

Jeongheon Kim

Korea Advanced Institute of Science and Technology

Nayoung Lee

Gyeongsang National University

Cooperative Institutions

Korea Advanced Institute of Science and Technology

Chungnam National University

Gyeongsang National University

Seoul National University

University of California, Riverside

Korea Research Institute of Bioscience and Biotechnology

Chonnam National University

Rural Development Administration

Korea Research Institute of Standards and Science

University of California, Davis

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Phytochrome and Ethylene Signaling Integration in Arabidopsis Occurs via the Transcriptional Regulation of Genes Co-targeted by PIFs and EIN3

Frontiers in Plant Science (2016)

Jinkil Jeong Keunhwa Kim Mi Eon Kim Hye Gi Kim Gwi Suk Heo

Plant seedlings germinating under the soil are challenged by rough soil grains that can induce physical damage and sudden exposure to light, which can induce photobleaching. Seedlings overcome these challenges by developing apical hooks and by suppressing chlorophyll precursor biosynthesis. These adaptive responses are, respectively, regulated by the phytochrome and ethylene signaling pathways via the PHYTOCHROME-INTERACTING FACTORs (PIFs) and the ETHYLENE INSENSITIVE 3 (EIN3)/EIN3-LIKE transcription factors. Although many processes downstream of phytochrome and ethylene signaling are similar, it remains unclear if and where these pathways converge. Here, we show PIFs and EIN3 induce similar changes in the transcriptome without robustly regulating each other's signaling pathways. PIFs and EIN3 target highly overlapped gene promoters and activate subsets of the co-target genes either interdependently or additively to induce plant responses. For chlorophyll biosynthesis, PIFs and EIN3 target and interdependently activate the expression of HOOKLESS1. HOOKLESS1, in turn, represses chlorophyll synthesis genes to prevent photobleaching. Thus, our results indicate an integration of the phytochrome and ethylene signaling pathways at the level of transcriptional gene regulation by two core groups of transcription factors, PIFs and EIN3.

Phytochrome

Transcription

10.3389/fpls.2016.01055

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Citations (28)

Phytochromes inhibit hypocotyl negative gravitropism by regulating the development of endodermal amyloplasts through phytochrome-interacting factors

Proceedings of the National Academy of Sciences (2011)

Keunhwa Kim Jieun Shin Sang Hee Lee Hee‐Seok Kweon Julin Maloof

Phytochromes are red and far-red light photoreceptors that regulate various aspects of plant development. One of the less-understood roles of phytochromes is the inhibition of hypocotyl negative gravitropism, which refers to the loss of hypocotyl gravitropism and resulting random growth direction in red or far-red light. This light response allows seedlings to curve toward blue light after emergence from the soil and enhances seedling establishment in the presence of mulch. Phytochromes inhibit hypocotyl negative gravitropism by inhibiting four phytochrome-interacting factors (PIF1, PIF3, PIF4, PIF5), as shown by hypocotyl agravitropism of dark-grown pif1 pif3 pif4 pif5 quadruple mutants. We show that phytochromes inhibit negative gravitropism by converting starch-filled gravity-sensing endodermal amyloplasts to other plastids with chloroplastic or etioplastic features in red or far-red light, whereas PIFs promote negative gravitropism by inhibiting the conversion of endodermal amyloplasts to etioplasts in the dark. By analyzing transgenic plants expressing PIF1 with an endodermis-specific SCARECROW promoter, we further show that endodermal PIF1 is sufficient to inhibit the conversion of endodermal amyloplasts to etioplasts and hypocotyl negative gravitropism of the pif quadruple mutant in the dark. Although the functions of phytochromes in gravitropism and chloroplast development are normally considered distinct, our results indicate that these two functions are closely related.

Gravitropism

Amyloplast

Phytochrome

Endodermis

Far-red

10.1073/pnas.1011066108

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Citations (85)

The Transcriptional Coregulator LEUNIG_HOMOLOG Inhibits Light-Dependent Seed Germination in Arabidopsis

The Plant Cell (2015)

Nayoung Lee Jeongmoo Park Keunhwa Kim Giltsu Choi

PHYTOCHROME-INTERACTING FACTOR1 (PIF1) is a basic helix-loop-helix transcription factor that inhibits light-dependent seed germination in Arabidopsis thaliana. However, it remains unclear whether PIF1 requires other factors to regulate its direct targets. Here, we demonstrate that LEUNIG_HOMOLOG (LUH), a Groucho family transcriptional corepressor, binds to PIF1 and coregulates its targets. Not only are the transcriptional profiles of the luh and pif1 mutants remarkably similar, more than 80% of the seeds of both genotypes germinate in the dark. We show by chromatin immunoprecipitation that LUH binds a subset of PIF1 targets in a partially PIF1-dependent manner. Unexpectedly, we found LUH binds and coregulates not only PIF1-activated targets but also PIF1-repressed targets. Together, our results indicate LUH functions with PIF1 as a transcriptional coregulator to inhibit seed germination.

Corepressor

Chromatin immunoprecipitation

Phytochrome

Transcription

10.1105/tpc.15.00444

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Citations (36)

PIF1 Regulates Plastid Development by Repressing Photosynthetic Genes in the Endodermis

Molecular Plant (2016)

Keunhwa Kim Jinkil Jeong Jeongheon Kim Nayoung Lee Mi Eon Kim

Amyloplast

Endodermis

Gravitropism

10.1016/j.molp.2016.08.007

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Citations (31)

Epidermal Phytochrome B Inhibits Hypocotyl Negative Gravitropism Non-Cell-Autonomously

The Plant Cell (2016)

Jaewook Kim Kijong Song Eunae Park Keunhwa Kim Gabyong Bae

Seedling hypocotyls display negative gravitropism in the dark but agravitropism in the light. The Arabidopsis thaliana pif quadruple mutant (pifQ), which lacks four PHYTOCHROME-INTERACTING FACTORS (PIFs), is agravitropic in the dark. Endodermis-specific expression of PIF1 rescues gravitropism in pifQ mutant seedlings. Since phytochromes induce light responses by inhibiting PIFs and the COP1-SPA ubiquitin E3 ligase complex in the nucleus, we asked whether phyB can cell autonomously inhibit hypocotyl negative gravitropism in the endodermis. We found that while epidermis-specific expression of PHYB rescues hypocotyl negative gravitropism and all other phyB mutant phenotypes, endodermis-specific expression of PHYB does not. Epidermal phyB induces the phosphorylation and degradation of endodermal PIFs in response to red light. This induces a global gene expression pattern similar to that induced by red light treatment of seedlings expressing PHYB under the control of its own endogenous promoter. Our results imply that epidermal phyB generates an unidentified mobile signal that travels to the endodermis where it promotes PIF degradation and inhibits hypocotyl negative gravitropism.

Gravitropism

Endodermis

10.1105/tpc.16.00487

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Citations (47)

HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis

FEBS Letters (2013)

Dong Ho Shin MyungGoo Choi Keunhwa Kim Geul Bang Misuk Cho

Several positive transcription factors regulate Arabidopsis anthocyanin biosynthesis. HY5, a component of light‐signaling pathways, and PAP1, an R2R3‐MYB transcription factor, share common regulatory targets on anthocyanin biosynthesis genes. The epistatic interactions between the two transcription factors are currently unknown. To address this problem, we analyzed crosses between hy5 and pap1 mutants ( hy5pap1 ) or pap1D overexpressors ( hy5pap1D ), performed chromatin immunoprecipitation‐qPCR, and determined the PAP1 promoter region through deletion analysis. The results show that HY5 regulates PAP1 expression via direct binding to G‐ and ACE‐boxes in the promoter region, which suggests bifurcate regulation of anthocyanin biosynthesis by HY5 via transcriptional activation of PAP1.

Chromatin immunoprecipitation

MYB

Transcription

10.1016/j.febslet.2013.03.037

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Citations (311)

Photobody formation spatially segregates two opposing phytochrome B signaling actions of PIF5 degradation and stabilization

Nature Communications (2024)

R KIM D. Fan Jiangman He Keunhwa Kim Juan Du

Abstract Photoactivation of the plant photoreceptor and thermosensor phytochrome B (PHYB) triggers its condensation into subnuclear membraneless organelles named photobodies (PBs). However, the function of PBs in PHYB signaling remains frustratingly elusive. Here, we found that PHYB recruits PHYTOCHROME-INTERACTING FACTOR 5 (PIF5) to PBs. Surprisingly, PHYB exerts opposing roles in degrading and stabilizing PIF5. Perturbing PB size by overproducing PHYB provoked a biphasic PIF5 response: while a moderate increase in PHYB enhanced PIF5 degradation, further elevating the PHYB level stabilized PIF5 by retaining more of it in enlarged PBs. Conversely, reducing PB size by dim light, which enhanced PB dynamics and nucleoplasmic PHYB and PIF5, switched the balance towards PIF5 degradation. Together, these results reveal that PB formation spatially segregates two antagonistic PHYB signaling actions – PIF5 stabilization in PBs and PIF5 degradation in the surrounding nucleoplasm – which could enable an environmentally sensitive, counterbalancing mechanism to titrate nucleoplasmic PIF5 and environmental responses.

Degradation

Phytochrome

Organelle

10.1038/s41467-024-47790-8

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Citations (3)

Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors

Proceedings of the National Academy of Sciences (2009)

Jieun Shin Keunhwa Kim Hyojin Kang Ismayil S. Zulfugarov Gabyong Bae

PIF3 is a phytochrome-interacting basic helix-loop-helix transcription factor that negatively regulates light responses, including hypocotyl elongation, cotyledon opening, and hypocotyl negative gravitropism. However, the role of PIF3 in chlorophyll biosynthesis has not been clearly defined. Here, we show that PIF3 also negatively regulates chlorophyll biosynthesis by repressing biosynthetic genes in the dark. Consistent with the gene expression patterns, the etiolated pif3 mutant accumulated a higher amount of protochlorophyllide and was bleached severely when transferred into light. The photobleaching phenotype of pif3 could be suppressed by the gun5 mutation and mimicked by overexpression of GUN5. When 4 negative phytochrome-interacting protein genes (PIF1, PIF3, PIF4, and PIF5) were mutated, the resulting quadruple mutant seedlings displayed constitutive photomorphogenic phenotypes, including short hypocotyls, open cotyledons, and disrupted hypocotyl gravitropism in the dark. Microarray analysis further confirmed that the dark-grown quadruple mutant has a gene expression pattern similar to that of red light-grown WT. Together, our data indicate that 4 phytochrome-interacting proteins are required for skotomorphogenesis and phytochromes activate photomorphogenesis by inhibiting these factors.

Phytochrome

Photomorphogenesis

Etiolation

Gravitropism

Phytochrome A

10.1073/pnas.0812219106

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Citations (474)

EARLY STARVATION 1 Is a Functionally Conserved Protein Promoting Gravitropic Responses in Plants by Forming Starch Granules

Frontiers in Plant Science (2021)

Kijong Song Dae-Woo Lee Jeongheon Kim Jaewook Kim Hwanuk Guim

Starch granules in the endodermis of plant hypocotyls act as statoliths that promote hypocotyl negative gravitropism-the directional growth of hypocotyls against gravity-in the dark. To identify the molecular components that regulate hypocotyl negative gravitropism, we performed a mutagenesis screen and isolated

10.3389/fpls.2021.628948

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Citations (10)

SlH3 and SlH4 promote multicellular Trichome formation and elongation by upregulating woolly in tomato

Horticulture Research (2025)

Seong-Min Kim Da‐Min Choi Jae-In Chun Seong-Yeop Kim Seong-Hyeon Kim

Trichome

Multicellular organism

Elongation

10.1093/hr/uhaf008

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Citations (0)