Skip to main content
Log in

Ds9 was isolated encoding as OsHAP3H and its C-terminus was required for interaction with HAP2 and HAP5

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Heading date is one of the most important agronomic traits in rice. Here, we analyzed an early flowering mutant ds9 under long day (LD) conditions and found that the early flowering phenotype was controlled by a single dominant gene. Mapping the Ds9 revealed that it was located near SSR marker RM5432 on chromosome 8, close to the known heading date-related DTH8/Ghd8 locus. Sequence analysis indicated that Ds9 was allelic to Ghd8, encoding the OsHAP3H subunit of CCAAT-box binding proteins (HAPs), and transformation of ds9 mutant with the OsHAP3H gene from wild type XS11 plants significantly increased the heading date under LD conditions. Yeast two hybrid and three hybrid assays revealed that the C-terminus of OsHAP3H is required for its interactions with OsHAP2 and OsHAP5. The data demonstrated that OsHAP3H plays a critical role as a repressor of photoperiodic flowering in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ballif J, Endo S, Kotani M, MacAdam J, Wu Y (2011) Over-expression of HAP3b enhances primary root elongation in Arabidopsis. Plant Physiol Biochem 49: 579–583

    Article  CAS  PubMed  Google Scholar 

  • Cai X, Ballif J, Endo S, Davis E, Liang M, Chen D, DeWald D, Kreps J, Zhu T, Wu Y (2007) A putative CCAAT-binding transcription factor is a regulator of flowering timing in Arabidopsis. Plant Physiol 145: 98–105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Calvenzani V, Testoni B, Gusmaroli G, Lorenzo M, Gnesutta N, Petroni K, Mantovani R, Tonelli C (2012) Interactions and CCAAT-binding of Arabidopsis thaliana NF-Y Subunits. PloS One 7: e42902

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dai X, Ding Y, Tan L, Fu Y, Liu F, Zhu Z, Sun X, Gu P, Cai H, Sun C (2012) LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J Integr Plant Biol 54: 790–799

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta S, Wood J, Hicks JB (1983) A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Gene Dev 18: 926–936

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dolfini D, Zambelli F, Pavesi G, Mantovani R (2009) A perspective of promoter architecture from the CCAAT box. Cell Cycle 8: 4127–4137

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Yamanouchi U, Yano M (2013) Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor Appl Genet 126:611–618

    Article  CAS  PubMed  Google Scholar 

  • Gusmaroli G, Tonelli C, Mantovani R (2001) Regulation of the CCAAT-binding NF-Y subunits in Arabidopsis thaliana. Gene 264:173–185

    Article  CAS  PubMed  Google Scholar 

  • Han X, Tang S, An Y, Zheng DC, Xia XL, Yin WL (2013) Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis. J Exp Bot 64:4589–4601

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol 135:677–684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces shortday flowering in rice. Nature 422:719–722

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Thirumurugan T, Serizawa A, Hiratsu K, Ohme-Takagi M, Kurata N (2011) Aberrant vegetative and reproductive development by overexpression and lethality by silencing of OsHAP3E in rice. Plant Sci 181:105–110

    Article  CAS  PubMed  Google Scholar 

  • Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat Genet 42:635–638

    Article  CAS  PubMed  Google Scholar 

  • Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091–3097

    Article  CAS  PubMed  Google Scholar 

  • Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Gene Dev 16:2006–2020

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34.

    Article  CAS  PubMed  Google Scholar 

  • Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) The nuclear factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228:709–723

    Article  CAS  PubMed  Google Scholar 

  • Kumimoto RW, Zhang Y, Siefers N, Holt BF (2010) NF-YC3, NFYC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J 63:379–391

    Article  CAS  PubMed  Google Scholar 

  • Kwong RW (2002) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18

    Article  Google Scholar 

  • Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2012) CCAATbox binding transcription factors in plants: Y so many? Trends Plant Sci 18:157–166

    Article  PubMed  Google Scholar 

  • Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239:15–27

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Ogiso-Tanaka E, Hori K, Ebana K, Ando T, Yano M (2012) Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol 53:709–716

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol 148:1425–1435

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540

    Article  CAS  PubMed  Google Scholar 

  • Nardini M, Gnesutta N, Donati G, Gatta R, Forni C, Fossati A, Vonrhein C, Moras D, Romier C, Bolognesi M, Mantovani R (2013) Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell 152:132–143

    Article  CAS  PubMed  Google Scholar 

  • Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on waterlimited acres. Proc Natl Acad Sci USA 104:16450–16455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, Xuan YH, Colasanti J, An G, Han CD (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J 56:1018–1029

    Article  CAS  PubMed  Google Scholar 

  • Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF, Mantovani R (2012) The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24:4777–4792

    Article  PubMed Central  PubMed  Google Scholar 

  • Saito H, Ogiso-Tanaka E, Okumoto Y, Yoshitake Y, Izumi H, Yokoo T, Matsubara K, Hori K, Yano M, Inoue H, Tanisaka T (2012) Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short- and long-day conditions. Plant Cell Physiol 53:717–728

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA 106:4555–4560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genom 279:279–289

    Article  CAS  Google Scholar 

  • Tsuji H, Taoka K, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52

    Article  CAS  PubMed  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  CAS  PubMed  Google Scholar 

  • Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18:2971–2984

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu C, You C, Li C, Long T, Chen G, Byrne ME, Zhang Q (2008) RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Natl Acad Sci USA 105:12915–12920

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hattori T (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABREbinding factors. Plant J 58:843–856

    Article  CAS  PubMed  Google Scholar 

  • Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH, Zhang YS, Yu SB, Xing YZ, Zhang QF (2011) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant 4:319–330

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Xue HW (2013) OsLEC1/OsHAP3E participates in the determination of meristem identity in both vegetative and reproductive developments of rice. J Integr Plant Biol 55:232–249

    Article  CAS  PubMed  Google Scholar 

  • Zheng KL, Huang N, Bennett J, Khush GS (1995) PCR-based markerassisted selection in rice breeding. In: IRRI discussionpaper series. No. 12. International Rice Research Institute, Manila, Philippines

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zejian Guo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xing, Q., Zheng, Z., Zhou, X. et al. Ds9 was isolated encoding as OsHAP3H and its C-terminus was required for interaction with HAP2 and HAP5. J. Plant Biol. 58, 26–37 (2015). https://doi.org/10.1007/s12374-014-0191-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-014-0191-1

Keywords

Navigation