Dynamic Antagonism between Phytochromes and PIF Family Basic Helix-Loop-Helix Factors Induces Selective Reciprocal Responses to Light and Shade in a Rapidly Responsive Transcriptional Network in <i>Arabidopsis</i>

Leivar, Pablo; Tepperman, James M.; Cohn, Megan; Monte, Elena; Al-Sady, Bassem; Erickson, Erika; Quail, Peter H.

doi:10.1105/tpc.112.095711

Cited by 207 publications

(259 citation statements)

References 84 publications

(218 reference statements)

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“…Long HYPOCOTYL IN FAR-RED1 (HFR1), PHY-TOCHROME RAPIDLY REGULATED1 (PAR1), and PAR2 are PIF4 targets genes and are transcriptionally induced by shade through a PIF-dependent mechanism (Leivar et al, 2012;Oh et al, 2012). Like IBH1, HFR1 and PAR1/PAR2 encode atypical bHLH proteins that lack DNA binding ability (Galstyan et al, 2011).…”

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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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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“…PIF transcription factors are negative regulators of red light signaling and promote scotomorphogenesis in dark-grown seedlings, controlling the expression of a large set of target genes (Leivar et al, 2012;Zhang et al, 2013). While transcript levels of PIF genes were not altered in ZFP3ox seedlings, many genes that were repressed or derepressed by ZFP3 overexpression were downand up-regulated in the quadruple pif1,3,4,5 mutant, respectively (Table III; Supplemental Data Sets S2-S5; Leivar et al, 2012). These data indicate that a subset of ZFP3-regulated genes are also targets of PIF-dependent transcriptional regulation, suggesting that ZFP3 and PIFs control an overlapping signaling pathway.…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis ZINC FINGER PROTEIN3 Interferes with Abscisic Acid and Light Signaling in Seed Germination and Plant Development

et al. 2014

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Seed germination is controlled by environmental signals, including light and endogenous phytohormones. Abscisic acid (ABA) inhibits, whereas gibberellin promotes, germination and early seedling development, respectively. Here, we report that ZFP3, a nuclear C2H2 zinc finger protein, acts as a negative regulator of ABA suppression of seed germination in Arabidopsis (Arabidopsis thaliana). Accordingly, regulated overexpression of ZFP3 and the closely related ZFP1, ZFP4, ZFP6, and ZFP7 zinc finger factors confers ABA insensitivity to seed germination, while the zfp3 zfp4 double mutant displays enhanced ABA susceptibility. Reduced expression of several ABA-induced genes, such as RESPONSIVE TO ABSCISIC ACID18 and transcription factor ABSCISIC ACID-INSENSITIVE4 (ABI4), in ZFP3 overexpression seedlings suggests that ZFP3 negatively regulates ABA signaling. Analysis of ZFP3 overexpression plants revealed multiple phenotypic alterations, such as semidwarf growth habit, defects in fertility, and enhanced sensitivity of hypocotyl elongation to red but not to far-red or blue light. Analysis of genetic interactions with phytochrome and abi mutants indicates that ZFP3 enhances red light signaling by photoreceptors other than phytochrome A and additively increases ABA insensitivity conferred by the abi2, abi4, and abi5 mutations. These data support the conclusion that ZFP3 and the related ZFP subfamily of zinc finger factors regulate light and ABA responses during germination and early seedling development.

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“…In the case of PIF3, these oscillations in protein levels are imposed by the action of phyA and phyB at dawn, which induce rapid degradation of PIF3 in response to light (dark-to-light transition) and by the action of phyB to maintain low levels of PIF3 at dusk and during early night (Soy et al, 2012). Phy regulation of PIF protein abundance is also observed in environments enriched in FR light, such as under vegetational shade, where there is a reduction in the R/FR ratio that imposes a shift in the phy photoequilibrium toward the Pr-inactive form, which results in rapid increases in PIF3, PIF4, and PIF5 protein levels Leivar et al, 2012b).…”

Section: Pif Function In Phy-mediated Growth Responses To Light Phy Rmentioning

confidence: 99%

“…Several excellent reviews have covered the role of PIFs in regulating phy-signaling and transcriptional networks Jeong and Choi, 2013) or have focused on their participation in specific processes, such as seed germination, shade avoidance, thermal-induced responses, or crosstalk with specific hormonal pathways or the circadian clock (Franklin, 2008;Lau and Deng, Leivar et al [2012b], Figure 1B.) 2010; Wang et al, 2012;Casal, 2013;de Wit et al, 2013;KinmonthSchultz et al, 2013;Proveniers and van Zanten, 2013;Shin et al, 2013;Wigge, 2013;Yamashino, 2013).…”

mentioning

confidence: 99%

PIFs: Systems Integrators in Plant Development

2014

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Dynamic Antagonism between Phytochromes and PIF Family Basic Helix-Loop-Helix Factors Induces Selective Reciprocal Responses to Light and Shade in a Rapidly Responsive Transcriptional Network in Arabidopsis

Cited by 207 publications

References 84 publications

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

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

The Arabidopsis ZINC FINGER PROTEIN3 Interferes with Abscisic Acid and Light Signaling in Seed Germination and Plant Development

PIFs: Systems Integrators in Plant Development

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