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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

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Abstract
Cell elongation is promoted by different environmental and hormonal signals, involving light, temperature, brassinosteroid (BR), and gibberellin, that inhibit the atypical basic helix-loop-helix (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.
Keywords
THALIANA, GROWTH, BHLH, GENE-EXPRESSION, SHADE AVOIDANCE, PLANT DEVELOPMENT, SIGNAL-TRANSDUCTION, growth, plant, RESPONSES, PHOTOMORPHOGENESIS, GIBBERELLIN, development

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MLA
Zhiponova, Miroslava, Kengo Morohashi, Isabelle Vanhoutte, et al. “Helix-loop-helix/basic Helix-loop-helix Transcription Factor Network Represses Cell Elongation in Arabidopsis Through an Apparent Incoherent Feed-forward Loop.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 111.7 (2014): 2824–2829. Print.
APA
Zhiponova, M., Morohashi, K., Vanhoutte, I., Machemer-Noonan, K., Revalska, M., Van Montagu, M., Grotewold, E., et al. (2014). Helix-loop-helix/basic helix-loop-helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 111(7), 2824–2829.
Chicago author-date
Zhiponova, Miroslava, Kengo Morohashi, Isabelle Vanhoutte, Katja Machemer-Noonan, Miglena Revalska, Marc Van Montagu, Erich Grotewold, and Eugenia Russinova. 2014. “Helix-loop-helix/basic Helix-loop-helix Transcription Factor Network Represses Cell Elongation in Arabidopsis Through an Apparent Incoherent Feed-forward Loop.” Proceedings of the National Academy of Sciences of the United States of America 111 (7): 2824–2829.
Chicago author-date (all authors)
Zhiponova, Miroslava, Kengo Morohashi, Isabelle Vanhoutte, Katja Machemer-Noonan, Miglena Revalska, Marc Van Montagu, Erich Grotewold, and Eugenia Russinova. 2014. “Helix-loop-helix/basic Helix-loop-helix Transcription Factor Network Represses Cell Elongation in Arabidopsis Through an Apparent Incoherent Feed-forward Loop.” Proceedings of the National Academy of Sciences of the United States of America 111 (7): 2824–2829.
Vancouver
1.
Zhiponova M, Morohashi K, Vanhoutte I, Machemer-Noonan K, Revalska M, Van Montagu M, et al. Helix-loop-helix/basic helix-loop-helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2014;111(7):2824–9.
IEEE
[1]
M. Zhiponova et al., “Helix-loop-helix/basic helix-loop-helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 111, no. 7, pp. 2824–2829, 2014.
@article{4350025,
  abstract     = {Cell elongation is promoted by different environmental and hormonal signals, involving light, temperature, brassinosteroid (BR), and gibberellin, that inhibit the atypical basic helix-loop-helix (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.},
  author       = {Zhiponova, Miroslava and Morohashi, Kengo and Vanhoutte, Isabelle and Machemer-Noonan, Katja and Revalska, Miglena and Van Montagu, Marc and Grotewold, Erich and Russinova, Eugenia},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keywords     = {THALIANA,GROWTH,BHLH,GENE-EXPRESSION,SHADE AVOIDANCE,PLANT DEVELOPMENT,SIGNAL-TRANSDUCTION,growth,plant,RESPONSES,PHOTOMORPHOGENESIS,GIBBERELLIN,development},
  language     = {eng},
  number       = {7},
  pages        = {2824--2829},
  title        = {Helix-loop-helix/basic helix-loop-helix transcription factor network represses cell elongation in Arabidopsis through an apparent incoherent feed-forward loop},
  url          = {http://dx.doi.org/10.1073/pnas.1400203111},
  volume       = {111},
  year         = {2014},
}

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