Skip to main content
Log in

Allelic variants of the esterase gene W14/15 differentially regulate overwinter survival in perennial gentian (Gentiana L.)

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

Abstract

Overwinter survival has to be under critical regulation in the lifecycle of herbaceous perennial plants. Gentians (Gentiana L.) maintain their perennial life style through producing dormant and freezing-tolerant overwinter buds (OWBs) to overcome cold winter. However, the mechanism acting on such an overwinter survival and the genes/proteins contributing to it have been poorly understood. Previously, we identified an OWB-enriched protein W14/15, a member of a group of α/β hydrolase fold superfamily that is implicated in regulation of hormonal action in plants. The W14/15 gene has more than ten variant types in Gentiana species. However, roles of the W14/15 gene in OWB survival and functional difference among those variants have been unclear. In the present study, we examined whether the W14/15 gene variants are involved in the mechanism acting on overwinter survival, by crossing experiments using cultivars carrying different W14/15 variant alleles and virus-induced gene silencing experiments. We found that particular types of the W14/15 variants (W15a types) contributed toward obtaining high ability of overwinter survival, while other types (W14b types) did not, or even interfered with the former type gene. This study demonstrates two findings; first, contribution of esterase genes to winter hardiness, and second, paired set or paired partner among the allelic variants determines the ability of overwinter survival.

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.

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

Similar content being viewed by others

References

  • Anderson JV, Dogramaci M, Horvath DP, Foley ME, Chao WS, Suttle JC, Thimmapuram J, Hernandez AG, Ali S, Mikel MA (2012) Auxin and ABA act as central regulators of developmental networks associated with paradormancy in Canada thistle (Cirsium arvense). Funct Integr Genom 12:515–531

    Article  CAS  Google Scholar 

  • Cooke JE, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728

    Article  CAS  PubMed  Google Scholar 

  • Doi H, Takahashi R, Hikage T, Takahata Y (2010) Embryogenesis and doubled haploid production from anther culture in gentian (Gentiana triflora). Plant Cell Tissue Organ Cult 102:27–33

    Article  Google Scholar 

  • Doi H, Yokoi S, Hikage T, Nishihara M, Tsutsumi K, Takahata Y (2011) Gynogenesis in gentians (Gentiana triflora, G. scabra): production of haploids and doubled haploids. Plant Cell Rep 30:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102:1773–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heikinheimo P, Goldman A, Jeffries C, Ollis DL (1999) Of barn owls and bankers: a lush variety of α/β hydrolases. Structure 7:R141–R146

    Article  CAS  PubMed  Google Scholar 

  • Hikage T, Saitoh Y, Tanaka-Saitoh C, Hagami H, Satou F, Shimotai Y, Nakano Y, Takahashi M, Takahata Y, Tsutsumi K (2007) Structure and allele-specific expression variation of novel alpha/beta hydrolase fold proteins in gentian plants. Mol Genet Genom 278:95–104

    Article  CAS  Google Scholar 

  • Hikage T, Kogusuri K, Tanaka-Saito C, Watanabe S, Chiba S, Kume K, Doi H, Saitoh Y, Takahata Y, Tsutsumi K (2011) W14/15 esterase gene haplotype can be a genetic landmark of cultivars and species of the genus Gentiana L. Mol Genet Genom 285:47–56

    Article  CAS  Google Scholar 

  • Ho TN, Liu SW (2001) A worldwide monograph of Gentiana. Science Press, Beijing, New York

    Google Scholar 

  • Horvath D (2009) Common mechanisms regulate flowering and dormancy. Plant Sci 177:523–531

    Article  CAS  Google Scholar 

  • Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JA (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L). BMC Genom 9:536

    Article  Google Scholar 

  • Imamura T, Nakatsuka T, Higuchi A, Nishihara M, Takahashi H (2011) The gentian orthologs of the FT/TFL1 gene family control floral initiation in Gentiana. Plant Cell Physiol 52:1031–1041

    Article  CAS  PubMed  Google Scholar 

  • Imamura T, Higuchi A, Takahashi H (2013) Dehydrins are highly expressed in overwintering buds and enhance drought and freezing tolerance in Gentiana triflora. Plant Sci 213:55–66

    Article  CAS  PubMed  Google Scholar 

  • Koehlein F (1991) GENTIANS. Christopher Helm Ltd, London

    Google Scholar 

  • Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100:16101–16106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortScience 22:371–377

    Google Scholar 

  • Mizutani M, Naganuma T, Tsutsumi K, Saitoh Y (2010) The syncytium specific expression of the Orysa;KRP3 CDK inhibitor: implication in its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm. J Exp Bot 61:791–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nardini M, Dijkstra BW (1999) Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 100:431–442

    Google Scholar 

  • Nishihara M, Nakatsuka T, Mizutani-Hukuchi M, Tanaka Y, Yamamura Y (2009) Gentians: from gene isolating to molecular breeding. In: Teixeria da Silva JA (ed) Floricultural and ornamental plant biotechnology V. Global Science Books, UK, pp 57–67

    Google Scholar 

  • Qin G, Gu H, Zhao Y, Ma Z, Shi G, Yang Y, Pichersky E, Chen H, Liu M, Chen Z, Qu LJ (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17:2693–2704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinne PLH, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26:249–264

    Article  CAS  PubMed  Google Scholar 

  • Ríos G, Leida C, Conejero A, Badenes ML (2014) Epigenetic regulation of bud dormancy events in perennial plants. Front Plant Sci 5:1–6

    Google Scholar 

  • Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223

    Article  CAS  PubMed  Google Scholar 

  • Stuhlfelder C, Mueller MJ, Warzecha H (2004) Cloning and expression of a tomato cDNA encoding a methyl jasmonate cleaving esterase. Eur J Biochem 271:2976–2983

    Article  CAS  PubMed  Google Scholar 

  • Takahashi M, Hikage T, Yamashita T, Saitoh Y, Endou M, Tsutsumi K (2006) Stress-related proteins are specifically expressed under non-stress conditions in the overwinter buds of the gentian plant Gentiana triflora. Breed Sci 56:39–46

    Article  CAS  Google Scholar 

  • Takahashi H, Imamura T, Konno N, Takeda T, Fujita K, Konishi T, Nishihara M, Uchimiya H (2014) The gentio-oligosaccharide gentiobiose functions in the mudulation of bud dormancy in the herbaceous perennial gentiana. Plant Cell 26:3949–3963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura A, Kato T, Taki A, Sone M, Satoh N, Yamagishi N, Takahashi T, Ryo B-S, Natsuaki T, Yoshikawa N (2013) Preventive and curative effects of Apple latent spherical virus vectors harboring part of the target virus genome against potyvirus and cucumovirus infections. Virology 446:314–324

    Article  CAS  PubMed  Google Scholar 

  • Tsutsumi K, Hikage T (2014) Genes expressed in the overwinter buds of Gentian (Gentiana spp.): application to taxonomic, phylogenetic and phylogeographical analyses. In: Rybczyński JJ, Davey MR, Mikuła A (eds) The gentianaceae, characterization and ecology, vol 1. Springer, Germany, pp 251–265

    Chapter  Google Scholar 

  • van der Schoot C, Rinne PLH (2012) Dormancy cycling at the apical meristem: transitioning between self-organizaton and self-arrest. Plant Sci 180:120–131

    Article  Google Scholar 

  • Yamagishi N, Yoshikawa N (2009) Virus-induced gene silencing in soybean seeds and the emergence stage of soybean plants with apple latent spherical virus vectors. Plant Mol Biol 71:15–24

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi N, Yoshikawa N (2011) Expression of FLOWERING LOCUS T from Arabidopsis thaliana induces precocious flowering in soybean irrespective of maturity group and stem growth habit. Planta 233:561–568

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi N, Sasaki S, Yamagata K, Komori S, Nagase M, Wada M, Yamamoto T, Yoshikawa N (2011) Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the apple latent spherical virus vector. Plant Mol Biol 75:193–204

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Xu R, Ma C-J, Vlot AC, Klessig DF, Pichersky E (2008) Inactive methyl indole-3-acetic acid can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol 147:1034–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshiike T (1992) Rindou (Gentiana). Seibunndou Shinkousha, Tokyo

    Google Scholar 

  • Zong GY, Goren R, Riov J, Sisler EC, Holland D (2001) Characterization of an ethylene-induced esterase from Citrus sinensis by competitive hybridization. Physiol Plant 113:267–274

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported in part by “Research and Development Projects for Application in Promoting New Policy of Agriculture, Forestry and Fisheries” from the Ministry of Agriculture, Forestry and Fisheries of Japan (to T.H. and K.T.), and by a grant-in-aid for scientific research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to K.T.). We thank Dr. K. Kume, S. Chiba, and Y. Endo for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ken-ichi Tsutsumi.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Nucleotide sequence data are available in the DDBJ/EMBL/GenBank Database under the accession numbers AB281493, AB281494, AB573233, AB573234, AB587674 and AB587675.

T. Hikage and N. Yamagishi contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hikage, T., Yamagishi, N., Takahashi, Y. et al. Allelic variants of the esterase gene W14/15 differentially regulate overwinter survival in perennial gentian (Gentiana L.). Mol Genet Genomics 291, 989–997 (2016). https://doi.org/10.1007/s00438-015-1160-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1160-1

Keywords

Navigation