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Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators

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Abstract
HISTONE MONOUBIQUITINATION1 (HUB1) and its paralog HUB2 act in a conserved heterotetrameric complex in the chromatin-mediated transcriptional modulation of developmental programs, such as flowering time, dormancy, and the circadian clock. The KHD1 and SPEN3 proteins were identified as interactors of the HUB1 and HUB2 proteins with in vitro RNA-binding activity. Mutants in SPEN3 and KHD1 had reduced rosette and leaf areas. Strikingly, in spen3 mutants, the flowering time was slightly, but significantly, delayed, as opposed to the early flowering time in the hub1-4 mutant. The mutant phenotypes in biomass and flowering time suggested a deregulation of their respective regulatory genes CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and FLOWERING LOCUS C (FLC) that are known targets of the HUB1-mediated histone H2B monoubiquitination (H2Bub). Indeed, in the spen3-1 and hub1-4 mutants, the circadian clock period was shortened as observed by luciferase reporter assays, the levels of the CCA1α and CCA1β splice forms were altered, and the CCA1 expression and H2Bub levels were reduced. In the spen3-1 mutant, the delay in flowering time was correlated with an enhanced FLC expression, possibly due to an increased distal versus proximal ratio of its antisense COOLAIR transcript. Together with transcriptomic and double-mutant analyses, our data revealed that the HUB1 interaction with SPEN3 links H2Bub during transcript elongation with pre-mRNA processing at CCA1 Furthermore, the presence of an intact HUB1 at the FLC is required for SPEN3 function in the formation of the FLC-derived antisense COOLAIR transcripts.
Keywords
H2Bub, HUB1 interactome, KH domain, RNA-binding protein, RRM domain

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Citation

Please use this url to cite or link to this publication:

Chicago
Woloszynska, Magdalena, Sabine Le Gall, Pia Neyt, Tommaso Matteo Boccardi, Marion Grasser, Gernot Längst, Stijn Aesaert, et al. 2019. “Histone 2B Monoubiquitination Complex Integrates Transcript Elongation with RNA Processing at Circadian Clock and Flowering Regulators.” Proceedings of the National Academy of Sciences of the United States of America 116 (16): 8060–8069.
APA
Woloszynska, M., Le Gall, S., Neyt, P., Boccardi, T. M., Grasser, M., Längst, G., Aesaert, S., et al. (2019). Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators. Proceedings of the National Academy of Sciences of the United States of America, 116(16), 8060–8069.
Vancouver
1.
Woloszynska M, Le Gall S, Neyt P, Boccardi TM, Grasser M, Längst G, et al. Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators. Proceedings of the National Academy of Sciences of the United States of America. Proceedings of the National Academy of Sciences; 2019;116(16):8060–9.
MLA
Woloszynska, Magdalena et al. “Histone 2B Monoubiquitination Complex Integrates Transcript Elongation with RNA Processing at Circadian Clock and Flowering Regulators.” Proceedings of the National Academy of Sciences of the United States of America 116.16 (2019): 8060–8069. Print.
@article{8611503,
  abstract     = {HISTONE MONOUBIQUITINATION1 (HUB1) and its paralog HUB2 act in a conserved heterotetrameric complex in the chromatin-mediated transcriptional modulation of developmental programs, such as flowering time, dormancy, and the circadian clock. The KHD1 and SPEN3 proteins were identified as interactors of the HUB1 and HUB2 proteins with in vitro RNA-binding activity. Mutants in SPEN3 and KHD1 had reduced rosette and leaf areas. Strikingly, in spen3 mutants, the flowering time was slightly, but significantly, delayed, as opposed to the early flowering time in the hub1-4 mutant. The mutant phenotypes in biomass and flowering time suggested a deregulation of their respective regulatory genes CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and FLOWERING LOCUS C (FLC) that are known targets of the HUB1-mediated histone H2B monoubiquitination (H2Bub). Indeed, in the spen3-1 and hub1-4 mutants, the circadian clock period was shortened as observed by luciferase reporter assays, the levels of the CCA1\ensuremath{\alpha} and CCA1\ensuremath{\beta} splice forms were altered, and the CCA1 expression and H2Bub levels were reduced. In the spen3-1 mutant, the delay in flowering time was correlated with an enhanced FLC expression, possibly due to an increased distal versus proximal ratio of its antisense COOLAIR transcript. Together with transcriptomic and double-mutant analyses, our data revealed that the HUB1 interaction with SPEN3 links H2Bub during transcript elongation with pre-mRNA processing at CCA1 Furthermore, the presence of an intact HUB1 at the FLC is required for SPEN3 function in the formation of the FLC-derived antisense COOLAIR transcripts.},
  author       = {Woloszynska, Magdalena and Le Gall, Sabine and Neyt, Pia and Boccardi, Tommaso Matteo and Grasser, Marion and L{\"a}ngst, Gernot and Aesaert, Stijn and Coussens, Griet and Dhondt, Stijn and Van De Slijke, Eveline and Bruno, Leonardo and Fung-Uceda, Jorge and Mas, Paloma and Van Montagu, Marc and Inz{\'e}, Dirk and Himanen, Kristiina and De Jaeger, Geert and Grasser, Klaus D. and Van Lijsebettens, Maria},
  issn         = {0027-8424},
  journal      = {Proceedings of the National Academy of Sciences of the United States of America},
  language     = {eng},
  number       = {16},
  pages        = {8060--8069},
  publisher    = {Proceedings of the National Academy of Sciences},
  title        = {Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators},
  url          = {http://dx.doi.org/10.1073/pnas.1806541116},
  volume       = {116},
  year         = {2019},
}

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