Skip to main content

Nucleoporin Nup98 participates in flowering regulation in a CONSTANS-independent mode

A Correction to this article was published on 21 February 2020

This article has been updated

Abstract

Key message

Two redundant nucleoporin genes Nup98a and Nup98b bypass the CO-check point in photoperiodic signaling and integrated signals from multiple pathways to directly target FT for flowering control in Arabidopsis.

Abstract

Flowering regulation is an important and widely studied plant development event. Even though nucleoporin Nup98 has been proven to play pivotal roles in the growth and development of mammalian cells and yeast, it is still unknown if Nup98 participates in flowering control in plants. In this study, we investigated the function of two Nup98 homologs, Nup98a and Nup98b, in flowering regulation in Arabidopsis. The results showed that Nup98a and Nup98b redundantly inhibit flowering through multiple pathways including clock, photoperiod, and age pathways. Single mutants of nup98a and nup98b do not show any obvious abnormal phenotypes compared to wild-type plants; however, the nup98a1 nup98b1 double mutant displays early flowering. Significantly, Nup98a/Nup98b gate flowering in a CONSTANS (CO)-independent mode. Therefore, Nup98a/Nup98b bypasses the CO checkpoint in photoperiodic signaling and integrated signals from multiple pathways to directly target FLOWERING LOCUS T (FT) for flowering control. In addition, our results provide a line of genetic evidence for uncoupling the mechanism of flowering and senescence at Nup98a/Nup98b genes in Arabidopsis, which are classically recognized as two coupled developmental events.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Change history

  • 21 February 2020

    The authors signal an error in Fig. 1b which does not show the correct set of plants and should be replaced with the included new figure.

  • 21 February 2020

    The authors signal an error in Fig.��1b which does not show the correct set of plants and should be replaced with the included new figure.

References

  • Andres F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639

    CAS  PubMed  Google Scholar 

  • Bouche F, Lobet G, Tocquin P, Perilleux C (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44:D1167–D1171

    CAS  PubMed  Google Scholar 

  • Braud C, Zheng W, Xiao W (2012) LONO1 encoding a nucleoporin is required for embryogenesis and seed viability in Arabidopsis. Plant Physiol 160:823–836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140:372–383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang Y, Li X (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503–2516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng JZ, Zhou YP, Lv TX, Xie CP, Tian CE (2017) Research progress on the autonomous flowering time pathway in Arabidopsis. Physiol Mol Biol Plants 23:477–485

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • Covington MF, Panda S, Liu XL, Strayer CA, Wagner DR, Kay SA (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13:1305–1315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26:9533–9543

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards KD, Millar AJ (2007) Analysis of circadian leaf movement rhythms in Arabidopsis thaliana. Methods Mol Biol 362:103–113

    PubMed  Google Scholar 

  • Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. Embo J 18:4679–4688

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gallemi M, Galstyan A, Paulisic S, Then C, Ferrandez-Ayela A, Lorenzo-Orts L, Roig-Villanova I, Wang X, Micol JL, Ponce MR, Devlin PF, Martinez-Garcia JF (2016) DRACULA2 is a dynamic nucleoporin with a role in regulating the shade avoidance syndrome in Arabidopsis. Development 143:1623–1631

    CAS  PubMed  Google Scholar 

  • Genenncher B, Wirthmueller L, Roth C, Klenke M, Ma L, Sharon A, Wiermer M (2016) Nucleoporin-regulated MAP kinase signaling in immunity to a necrotrophic fungal pathogen. Plant Physiology 172:1293–1305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffis ER, Altan N, Lippincott-Schwartz J, Powers MA (2002) Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 13:1282–1297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffis ER, Xu S, Powers MA (2003) Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol Biol Cell 14:600–610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez L, Mauriat M, Guenin S, Pelloux J, Lefebvre JF, Louvet R, Rusterucci C, Moritz T, Guerineau F, Bellini C, Van Wuytswinkel O (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol J 6:609–618

    CAS  PubMed  Google Scholar 

  • Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249

    CAS  PubMed  Google Scholar 

  • Jacob Y, Mongkolsiriwatana C, Veley KM, Kim SY, Michaels SD (2007) The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiol 144:1383–1390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johansson M, Staiger D (2015) Time to flower: interplay between photoperiod and the circadian clock. J Exper Botany 66:719–730

    CAS  Google Scholar 

  • Kalverda B, Pickersgill H, Shloma VV, Fornerod M (2010) Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140:360–371

    CAS  PubMed  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364

    CAS  PubMed  Google Scholar 

  • Kim H, Kim HJ, Vu QT, Jung S, McClung CR, Hong S, Nam HG (2018a) Circadian control of ORE1 by PRR9 positively regulates leaf senescence in Arabidopsis. Proc Natl Acad Sci USA 115:8448–8453

    CAS  PubMed  Google Scholar 

  • Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018b) New insights into the regulation of leaf senescence in Arabidopsis. J Exper Botany 69:787–799

    CAS  Google Scholar 

  • McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–720

    CAS  PubMed  Google Scholar 

  • Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carre IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641

    CAS  PubMed  Google Scholar 

  • Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15:2308–2319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nature Struct Mol Biol 23:1061–1069

    CAS  Google Scholar 

  • Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285:1579–1582

    CAS  PubMed  Google Scholar 

  • Parry G (2014) Components of the Arabidopsis nuclear pore complex play multiple diverse roles in control of plant growth. J Exp Bot 65:6057–6067

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parry G, Ward S, Cernac A, Dharmasiri S, Estelle M (2006) The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signaling and development. Plant Cell 18:1590–1603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robles LM, Deslauriers SD, Alvarez AA, Larsen PB (2012) A loss-of-function mutation in the nucleoporin AtNUP160 indicates that normal auxin signalling is required for a proper ethylene response in Arabidopsis. J Exp Bot 63:2231–2241

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148:635–651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:11698–11703

    CAS  PubMed  Google Scholar 

  • Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229

    CAS  PubMed  Google Scholar 

  • Shim JS, Kubota A, Imaizumi T (2017) Circadian clock and photoperiodic flowering in Arabidopsis: CONSTANS is a hub for signal integration. Plant Physiol 173:5–15

    CAS  PubMed  Google Scholar 

  • Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464

    CAS  PubMed  Google Scholar 

  • Strambio-De-Castillia C, Niepel M, Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11:490–501

    CAS  PubMed  Google Scholar 

  • Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. The Plant cell 22:4084–4097

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang M, Ning Y, Shu X, Dong B, Zhang H, Wu D, Wang H, Wang GL, Zhou B (2017) The Nup98 homolog APIP12 targeted by the effector AvrPiz-t is involved in rice basal resistance against magnaporthe oryzae. Rice (N Y) 10:5

    Google Scholar 

  • Upadhyay RK, Gupta A, Ranjan S, Singh R, Pathre UV, Nath P, Sane AP (2014) The EAR motif controls the early flowering and senescence phenotype mediated by over-expression of SlERF36 and is partly responsible for changes in stomatal density and photosynthesis. PloS One 9:e101995

    PubMed  PubMed Central  Google Scholar 

  • Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4723–4730

    CAS  PubMed  Google Scholar 

  • Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217

    CAS  PubMed  Google Scholar 

  • Wang X, Fan C, Zhang X, Zhu J, Fu YF (2013) BioVector, a flexible system for gene specific-expression in plants. BMC Plant Biol 13:198

    PubMed  PubMed Central  Google Scholar 

  • Weis K (2003) Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112:441–451

    CAS  PubMed  Google Scholar 

  • Wiermer M, Cheng YT, Imkampe J, Li M, Wang D, Lipka V, Li X (2012) Putative members of the Arabidopsis Nup107-160 nuclear pore sub-complex contribute to pathogen defense. Plant J 70:796–808

    CAS  PubMed  Google Scholar 

  • Xiao C, Chen F, Yu X, Lin C, Fu YF (2009) Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol Biol 71:39–50

    CAS  PubMed  Google Scholar 

  • Xiao L, Liu W, Chen F, Zhang X, Chen Q, Fu Y-F (2016) The phenotype analysis of NUP107-160 subcomplex mutants in Arabidopsis. J Agri Sci Tech 18:54–61 (In Chinese with English Abstract)

    Google Scholar 

  • Xu XM, Rose A, Muthuswamy S, Jeong SY, Venkatakrishnan S, Zhao Q, Meier I (2007) NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19:1537–1548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates suppressor of overexpression of CONSTANS 1 through Flowering Locus T to promote flowering in Arabidopsis. Plant Physiol 139:770–778

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Li X (2005) A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1. The Plant cell 17:1306–1316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Q, Meier I (2011) Identification and characterization of the Arabidopsis FG-repeat nucleoporin Nup62. Plant Signal Behavior 6:330–334

    CAS  Google Scholar 

Download references

Acknowledgements

We thank all friends and colleagues who help us but are not included in the author list. This research was supported by the National Natural Science Foundation of China (Grant nos. 31571411 and 31370324), CAAS-Innovation Team Project and the Basal Research Fund of CAAS (Y2017CG25). We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Author information

Affiliations

Authors

Contributions

Conceptualization, XZ and Y-FF; methodology, Y-FF, SJ, and LX; investigation, SJ, LX, FC, PH, ZC, and YM; formal analysis and validation, SJ, LX, and Y-FF; visualization, Y-FF; and writing, Y-FF, XZ, and QC. Funding acquisition, Y-FF and XZ; project administration, Y-FF, XZ, and QC; and supervision, Y-FF.

Corresponding authors

Correspondence to Yong-Fu Fu, Qingshan Chen or Xiao-Mei Zhang.

Ethics declarations

Conflict of interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Rachel Wells.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jiang, S., Xiao, L., Huang, P. et al. Nucleoporin Nup98 participates in flowering regulation in a CONSTANS-independent mode. Plant Cell Rep 38, 1263–1271 (2019). https://doi.org/10.1007/s00299-019-02442-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-019-02442-w

Keywords

  • Nuclear pore complex
  • Nucleoporin
  • Nup98
  • Flowering
  • CONSTANS
  • FLOWERING LOCUS T
  • Arabidopsis