A Triantagonistic Basic Helix-Loop-Helix System Regulates Cell Elongation in <i>Arabidopsis</i>

Ikeda, Miho; Fujiwara, Shigeru; Mitsuda, Nobutaka; Ohme‐Takagi, Masaru

doi:10.1105/tpc.112.105023

Cited by 159 publications

(167 citation statements)

References 43 publications

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“…The expression of a small group of genes peaked at 45 min ( Figure 6C, purple cluster). Notably, this group includes the gene ILI1 BINDING BHLH1, encoding a small HLH protein that was previously shown to regulate hypocotyl elongation (Bai et al, 2012;Ikeda et al, 2012). Among the genes whose expression peaked at 90 min ( Figure 6C, blue cluster), several terms associated with hormone pathways were enriched (Supplemental Data Set 8).…”

Section: Shade Treatment Leads To a Strong Genomic Signature Of Enhanmentioning

confidence: 95%

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

et al. 2016

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ORCID IDs: 0000-0001-5075-575X (M.V.K.); 0000-0003-1339-5120 (E.S.-S.); 0000-0002-4145-7205 (F.S.); 0000-0001-9237-1797 (P.M.-M.); 0000-0002-9623-2599 (J.M.); 0000-0002-3413-6841 (I.X.); 0000-0003-4719-5901 (C.F.)In response to neighbor proximity, plants increase the growth of specific organs (e.g., hypocotyls) to enhance access to sunlight. Shade enhances the activity of Phytochrome Interacting Factors (PIFs) by releasing these bHLH transcription factors from phytochrome B-mediated inhibition. PIFs promote elongation by inducing auxin production in cotyledons. In order to elucidate spatiotemporal aspects of the neighbor proximity response, we separately analyzed gene expression patterns in the major light-sensing organ (cotyledons) and in rapidly elongating hypocotyls of Arabidopsis thaliana. PIFs initiate transcriptional reprogramming in both organs within 15 min, comprising regulated expression of several early auxin response genes. This suggests that hypocotyl growth is elicited by both local and distal auxin signals. We show that cotyledon-derived auxin is both necessary and sufficient to initiate hypocotyl growth, but we also provide evidence for the functional importance of the local PIFinduced response. With time, the transcriptional response diverges increasingly between organs. We identify genes whose differential expression may underlie organ-specific elongation. Finally, we uncover a growth promotion gene expression signature shared between different developmentally regulated growth processes and responses to the environment in different organs.

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Section: Shade Treatment Leads To a Strong Genomic Signature Of Enhanmentioning

confidence: 95%

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

et al. 2016

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“…However, overexpression of BEE1 enhanced BR response only in root but caused no obvious hypocotyl phenotype. Yeast two-hybrid assays showed that IBH1 interacts with not only HBI1 but also BEE2 and seven additional homologous bHLHs (see Supplemental Figure 2 online; Ikeda et al, 2012). BEE2 and these other bHLH factors may play redundant roles with HBI1, and BR may regulate their activities at transcriptional and/or posttranslational levels.…”

Section: Discussionmentioning

confidence: 99%

A Triple Helix-Loop-Helix/Basic Helix-Loop-Helix Cascade Controls Cell Elongation Downstream of Multiple Hormonal and Environmental Signaling Pathways inArabidopsis

et al. 2012

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Environmental and endogenous signals, including light, temperature, brassinosteroid (BR), and gibberellin (GA), regulate cell elongation largely by influencing the expression of the paclobutrazol-resistant (PRE) family helix-loop-helix (HLH) factors, which promote cell elongation by interacting antagonistically with another HLH factor, IBH1. However, the molecular mechanism by which PREs and IBH1 regulate gene expression has remained unknown. Here, we show that IBH1 interacts with and inhibits a DNA binding basic helix-loop-helix (bHLH) protein, HBI1, in Arabidopsis thaliana. Overexpression of HBI1 increased hypocotyl and petiole elongation, whereas dominant inactivation of HBI1 and its homologs caused a dwarf phenotype, indicating that HBI1 is a positive regulator of cell elongation. In vitro and in vivo experiments showed that HBI1 directly bound to the promoters and activated two EXPANSIN genes encoding cell wall-loosening enzymes; HBI1's DNA binding and transcriptional activities were inhibited by IBH1, but the inhibitory effects of IBH1 were abolished by PRE1. The results indicate that PREs activate the DNA binding bHLH factor HBI1 by sequestering its inhibitor IBH1. Altering each of the three factors affected plant sensitivities to BR, GA, temperature, and light. Our study demonstrates that PREs, IBH1, and HBI1 form a chain of antagonistic switches that regulates cell elongation downstream of multiple external and endogenous signals.

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“…HBI1, ACE1, ACE2, ACE3, and CIB1 positively regulate cell elongation downstream of BRs, GAs, temperature, and light signaling. ACE1 and HBI1 activate directly elongation-promoting genes, such as EXPANSIN and XYLOGLUCAN ENDOTRANSGLYCOSYLASE/HYDROLASE (5,6). Whereas IBH1 interacts with HBI1 and ACE1 to inhibit their binding to DNA, PRE1 binds to IBH1 to prevent its repressive effect on HBI1 or ACE1, thus activating it.…”

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confidence: 99%

“…This regulatory mechanism involves activation of members of the PACLOBUTRAZOL RESISTANCE (PRE) family of atypical basic helix-loop-helix (bHLH) transcription factors (1)(2)(3)(4)(5)(6). PRE members are helix-loop-helix (HLH) proteins that lack the basic domain required for DNA binding and antagonize their interacting HLH or bHLH proteins, of which most act as cell elongation suppressors, thus forming triantagonistic bHLH systems (5,6). An example of such a system is the Arabidopsis thaliana PRE1 and its interactor, the HLH factor INCREASED LEAF INCLINATION1 BINDING bHLH1 (IBH1).…”

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confidence: 99%

“…Both BZR1 and BZR2/BES1 bind the IBH1 promoter to repress it (10,11). IBH1 does not bind DNA directly but interacts with the DNA binding bHLH factors HOMOLOG OF BR-ENHANCED EXPRESSION2 (BEE2), INTERACTING WITH IBH1 (HBI1), ACTIVATOR FOR CELL ELONGATION1 (ACE1), ACE2, ACE3, and CRYPTOCHROME INTERACTING bHLH1 (CIB1) (5,6). HBI1, ACE1, ACE2, ACE3, and CIB1 positively regulate cell elongation downstream of BRs, GAs, temperature, and light signaling.…”

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confidence: 99%

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Helix–loop–helix/basic helix–loop–helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop

Zhiponova

Morohashi

Vanhoutte

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Cell elongation is promoted by different environmental and hormonal signals, involving light, temperature, brassinosteroid (BR), and gibberellin, that inhibit the atypical basic helix-loophelix (bHLH) transcription factor INCREASED LEAF INCLINATION1 BINDING bHLH1 (IBH1). Ectopic accumulation of IBH1 causes a severe dwarf phenotype, but the cell elongation suppression mechanism is still not well understood. Here, we identified a close homolog of IBH1, IBH1-LIKE1 (IBL1), that also antagonized BR responses and cell elongation. Genome-wide expression analyses showed that IBH1 and IBL1 act interdependently downstream of the BRASSINAZOLE-RESISTANT1 (BZR1)-PHYTOCHROME-INTERACTING FACTOR 4 (PIF4)-DELLA module. Although characterized as non-DNA binding, IBH1 repressed direct IBL1 transcription, and they both acted in tandem to suppress the expression of a common downstream helix-loop-helix (HLH)/bHLH network, thus forming an incoherent feed-forward loop. IBH1 and IBL1 together repressed the expression of PIF4, known to stimulate skotomorphogenesis synergistically with BZR1. Strikingly, PIF4 bound all direct and down-regulated HLH/bHLH targets of IBH1 and IBL1. Additional genome-wide comparisons suggested a model in which IBH1 antagonized PIF4 but not the PIF4-BZR1 dimer.development | plant | growth

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A Triantagonistic Basic Helix-Loop-Helix System Regulates Cell Elongation in Arabidopsis

Cited by 159 publications

References 43 publications

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

A Triple Helix-Loop-Helix/Basic Helix-Loop-Helix Cascade Controls Cell Elongation Downstream of Multiple Hormonal and Environmental Signaling Pathways inArabidopsis

Helix–loop–helix/basic helix–loop–helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop

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