Skip to main content
SpringerLink
Log in

Conservation and divergence of plant LHP1 protein sequences and expression patterns in angiosperms and gymnosperms

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Floral transition is a critical and strictly regulated developmental process in plants. Mutations in Arabidopsis LIKE HETEROCHROMATIN PROTEIN 1 (AtLHP1)/TERMINAL FLOWER 2 (TFL2) result in early and terminal flowers. Little is known about the gene expression, function and evolution of plant LHP1 homologs, except for Arabidopsis LHP1. In this study, the conservation and divergence of plant LHP1 protein sequences was analyzed by sequence alignments and phylogeny. LHP1 expression patterns were compared among taxa that occupy pivotal phylogenetic positions. Several relatively conserved new motifs/regions were identified among LHP1 homologs. Phylogeny of plant LHP1 proteins agreed with established angiosperm relationships. In situ hybridization unveiled conserved expression of plant LHP1 in the axillary bud/tiller, vascular bundles, developing stamens, and carpels. Unlike AtLHP1, cucumber CsLHP1-2, sugarcane SoLHP1 and maize ZmLHP1, rice OsLHP1 is not expressed in the shoot apical meristem (SAM) and the OsLHP1 transcript level is consistently low in shoots. “Unequal crossover” might have contributed to the divergence in the N-terminal and hinge region lengths of LHP1 homologs. We propose an “insertion–deletion” model for soybean (Glycine max L.) GmLHP1s evolution. Plant LHP1 homologs are more conserved than previously expected, and may favor vegetative meristem identity and primordia formation. OsLHP1 may not function in rice SAM during floral induction.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22(5):1425–1440

    Article  PubMed  CAS  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242

    Article  PubMed  Google Scholar 

  • Bai SL, Peng YB, Cui JX, Gu HT, Xu LY, Li YQ, Xu ZH, Bai SN (2004) Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.). Planta 220:230–240

    Article  PubMed  CAS  Google Scholar 

  • Barrero JM, Gonzalez-Bayon R, Del PJ, Ponce MR, Micol JL (2007) INCURVATA2 encodes the catalytic subunit of DNA Polymerase alpha and interacts with genes involved in chromatin-mediated cellular memory in Arabidopsis thaliana. Plant Cell 19:2822–2838

    Article  PubMed  CAS  Google Scholar 

  • Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125(4):655–664

    Article  PubMed  Google Scholar 

  • Burleigh JG, Hilu KW, Soltis DE (2009) Inferring phylogenies with incomplete data sets: a 5-gene, 567-taxon analysis of angiosperms. BMC Evol Biol 9:61

    Article  PubMed  Google Scholar 

  • Churchman ML, Brown ML, Kato N, Kirik V, Hulskamp M, Inze D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, Gwin T, Churchman J, Larkin JC (2006) SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18:3145–3157

    Article  PubMed  CAS  Google Scholar 

  • Cui H, Benfey PN (2009) Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. Plant J 58:1016–1027

    Article  PubMed  CAS  Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, DePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    Article  PubMed  CAS  Google Scholar 

  • Daniell H, Wurdack KJ, Kanagaraj A, Lee SB, Saski C, Jansen RK (2008) The complete nucleotide sequence of the cassava (Manihot esculenta) chloroplast genome and the evolution of atpF in Malpighiales: RNA editing and multiple losses of a group II intron. Theor Appl Genet 116:723–737

    Article  PubMed  CAS  Google Scholar 

  • Del OI, Lopez-Gonzalez L, Martin-Trillo MM, Martinez-Zapater JM, Pineiro M, Jarillo JA (2010) EARLY IN SHORT DAYS 7 (ESD7) encodes the catalytic subunit of DNA polymerase epsilon and is required for flowering repression through a mechanism involving epigenetic gene silencing. Plant J 61:623–636

    Article  Google Scholar 

  • Exner V, Aichinger E, Shu H, Wildhaber T, Alfarano P, Caflisch A, Gruissem W, Kohler C, Hennig L (2009) The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS One 4(4):e5335

    Article  PubMed  Google Scholar 

  • Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128:4847–4858

    PubMed  CAS  Google Scholar 

  • Glémin S, Bataillon T (2009) A comparative view of the evolution of grasses under domestication. New Phytol 183(2):273–290

    Article  PubMed  Google Scholar 

  • Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. John Wiley & Sons, Inc, New York

  • Gough J (2005) Convergent evolution of domain architectures (is rare). Bioinformatics 21:1464–1471

    Article  PubMed  CAS  Google Scholar 

  • Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot 103:1165–1172

    Article  PubMed  CAS  Google Scholar 

  • APG (Angiosperm Phylogeny Group) (1998) An ordinal classification for the families of flowering plants. Ann Mo Bot Gard 85(4):531–533

    Google Scholar 

  • He Y (2009) Control of the transition to flowering by chromatin modifications. Mol Plant 2:554–564

    Article  PubMed  CAS  Google Scholar 

  • Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414–423

    Article  PubMed  CAS  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  PubMed  CAS  Google Scholar 

  • Jacquemin J, Laudie M, Cooke R (2009) A recent duplication revisited: phylogenetic analysis reveals an ancestral duplication highly-conserved throughout the Oryza genus and beyond. BMC Plant Biol 9:146

    Article  PubMed  Google Scholar 

  • Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Durrett TP, Last RL, Jander G (2004) Characterization of the Arabidopsis TU8 glucosinolate mutation, an allele of TERMINAL FLOWER2. Plant Mol Biol 54:671–682

    Article  PubMed  CAS  Google Scholar 

  • Kim KD, Shin JH, Van K, Kim DH, Lee SH (2009) Dynamic rearrangements determine genome organization and useful traits in soybean. Plant Physiol 151:1066–1076

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Weigel D (2007) Move on up, it’s time for change—mobile signals controlling photoperiod-dependent flowering. Genes Dev 21(19):2371–2384

    Article  PubMed  CAS  Google Scholar 

  • Kotake T, Takada S, Nakahigashi K, Ohto M, Goto K (2003) Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol 44:555–564

    Article  PubMed  CAS  Google Scholar 

  • Larsson AS, Landberg K, Meeks-Wagner DR (1998) The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana. Genetics 149:597–605

    PubMed  CAS  Google Scholar 

  • Libault M, Tessadori F, Germann S, Snijder B, Fransz P, Gaudin V (2005) The Arabidopsis LHP1 protein is a component of euchromatin. Planta 222:910–925

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16:711–722

    Article  PubMed  CAS  Google Scholar 

  • Luo C, Durgin BG, Watanabe N, Lam E (2009a) Defining the functional network of epigenetic regulators in Arabidopsis thaliana. Mol Plant 2:661–674

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES (2009b) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2:711–723

    Article  PubMed  CAS  Google Scholar 

  • Mimida N, Kidou S, Kotoda N (2007) Constitutive expression of two apple (Malus × domestica Borkh.) homolog genes of LIKE HETEROCHROMATIN PROTEIN1 affects flowering time and whole-plant growth in transgenic Arabidopsis. Mol Genet Genomics 278:295–305

    Article  PubMed  CAS  Google Scholar 

  • Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363–19368

    Article  PubMed  Google Scholar 

  • Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L, Bernatavichute YV, Jacobsen SE, Fransz P, Dean C (2006) LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc Natl Acad Sci USA 103:5012–5017

    Article  PubMed  CAS  Google Scholar 

  • Nakahigashi K, Jasencakova Z, Schubert I, Goto K (2005) The Arabidopsis heterochromatin protein1 homolog (TERMINAL FLOWER2) silences genes within the euchromatic region but not genes positioned in heterochromatin. Plant Cell Physiol 46:1747–1756

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  PubMed  CAS  Google Scholar 

  • Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512

    Article  PubMed  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  PubMed  CAS  Google Scholar 

  • Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38:706–710

    Article  PubMed  CAS  Google Scholar 

  • Takada S, Goto K (2003) Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell 15:2856–2865

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86

    Article  PubMed  Google Scholar 

  • Wijeratne AJ, Zhang W, Sun Y, Liu W, Albert R, Zheng Z, Oppenheimer DG, Zhao D, Ma H (2007) Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. Plant J 52:14–29

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Shen WH (2008) Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18:1966–1971

    Article  PubMed  CAS  Google Scholar 

  • Zemach A, Li Y, Ben-Meir H, Oliva M, Mosquna A, Kiss V, Avivi Y, Ohad N, Grafi G (2006) Different domains control the localization and mobility of LIKE HETEROCHROMATIN PROTEIN1 in Arabidopsis nuclei. Plant Cell 18:133–145

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 lys-27 trimethylation. Nat Struct Mol Biol 14:869–871

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by generous funding from The Floral Genome Project (FGP No. 0115684) to DGO, and the Ministry of Science and Technology of China (NSFC No. 30860127) and Guangxi Science Foundation (GSF No. 0731002) to HG. We thank the PSU and Prof. Douglas E. Soltis (Department of Biology, University of Florida, Gainesville, FL 32611) for providing clones and plant materials, Dr. Lars Hennig (Department of Biology & Zurich-Basel Plant Science Center, ETH Zurich, Zurich, Switzerland) for kindly providing the PpLHP1 and SmLHP1 sequences, Dr. Litao Yang (Agricultural college, Guangxi University, Nanning, 530004, China) for providing sugarcane materials, and Dr. Xiaoqin Hao (Agricultural college, Guangxi University, Nanning, 530004, China) for providing maize materials. Last but not least we thank the anonymous reviewers for their critical reading of this manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, UF Genetics Institute, Plant Molecular & Cellular Biology Program, University of Florida, 220 Bartram Hall, PO Box 118526, Gainesville, FL, 32611, USA

    Hexin Guan, Zhengui Zheng, Paris H. Grey & David G. Oppenheimer

  2. Agricultural College, Guangxi University, Nanning, 530004, China

    Hexin Guan & Yuhua Li

Authors
  1. Hexin Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhengui Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paris H. Grey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuhua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David G. Oppenheimer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David G. Oppenheimer.

Additional information

Communicated by A. Tyagi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

438_2011_609_MOESM1_ESM.ppt

Fig. S1A Alignment of LHP1 homologs for in-situ-hybridization studies. Highly conserved domains/motifs are indicated as in Mimida et al. (2007). Gymnosperms and Poaceae specific motifs are highlighted with red and blue boxes, respectively. The CsLHP1-2 sequence used in the alignment is cloned in the present study. (PPT 132 kb)

438_2011_609_MOESM2_ESM.ppt

Fig. S1B Phylogenetic tree for in-situ-hybridization studies. Numbers along branches are bootstrap values (1,000 replicates). (PPT 164 kb)

438_2011_609_MOESM3_ESM.ppt

Fig. S2 Conservation and divergence of LHP1 homologs at the N-terminal region. K/R and core E/D motif, as well as the N-terminal region are indicated. (PPT 159 kb)

438_2011_609_MOESM4_ESM.ppt

Fig. S3 Conservation and divergence of HP1 homologs at the N-terminal region. K/R and E/D motif were marked. HP1 homologs were selected according to Exner et al. (2009). (PPT 103 kb)

(jpg 530 kb)

438_2011_609_MOESM6_ESM.xls

Table S1 Identity analysis of GmLHP1-16. Original identity data were retrieved based on Fig. 2 through DNAMAN, transformed (Sheet 1), and statistical analysis (Sheet 2) was conducted according to Gomez et al. (1984). (XLS 56 kb)

438_2011_609_MOESM7_ESM.ppt

Table S2 Contribution of amino acid residue loss from diverged regions to whole residue loss in GmLHP1-04, GmLHP1-06 and MtLHP1-03. The number of amino acid residues within the diverged regions was calculated according to Fig. 2. Values were normalized with GmLHP1-16 counterpart values through y=(x-435)/435×100% in column a, y=(x-231)/231×100% in column b, and y= residues loss within diverged regions/whole residues loss (compared to GmLHP1-16) ×100% in column c, respectively. (PPT 87 kb)

Accession numbers (sequences) (DOC 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guan, H., Zheng, Z., Grey, P.H. et al. Conservation and divergence of plant LHP1 protein sequences and expression patterns in angiosperms and gymnosperms. Mol Genet Genomics 285, 357–373 (2011). https://doi.org/10.1007/s00438-011-0609-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-011-0609-0

Keywords

Search

Navigation