Skip to main content
SpringerLink
Log in

Apple latent spherical virus vector-induced flowering for shortening the juvenile phase in Japanese gentian and lisianthus plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Infection by apple latent spherical virus (ALSV) vectors that promote the expression of Arabidopsis thaliana FLOWERING LOCUS T ( AtFT ) or Gentiana triflora GtFT s accelerates flowering in gentian and lisianthus plants.

Apple latent spherical virus (ALSV) has isometric virus particles (25 nm in diameter) that contain two ssRNA species (RNA1 and RNA2) and three capsid proteins (Vp25, Vp20, and Vp24). ALSV vectors are used for foreign gene expression and virus-induced gene silencing in a broad range of plant species. Here, we report the infection by ALSV vectors that express FLOWERING LOCUS T (AtFT) from Arabidopsis thaliana or its homolog GtFT1 from Gentiana triflora in three gentian cultivars (‘Iwate Yume Aoi’ [early flowering], ‘Iwate’ [medium flowering], and ‘Alta’ [late flowering]), and two lisianthus cultivars (‘Newlination Pink ver. 2’ and ‘Torukogikyou daburu mikkusu’) promotes flowering within 90 days post-inoculation using particle bombardment. Additionally, seedlings from the progeny of the early-flowering plants were tested by tissue blot hybridization, and the results showed that ALSV was not transmitted to the next generation. The promotion of flowering in the family Gentianaceae by ALSV vectors shortened the juvenile phase from 1–3 years to 3–5 months, and thus, it could be considered as a new plant breeding technique in ornamental gentian and lisianthus plants.

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

Similar content being viewed by others

Abbreviations

ALSV:

Apple latent spherical virus

AtFT:

Arabidopsis thaliana FLOWERING LOCUS T

Dpi:

Days post-inoculation

GtFT:

Gentiana triflora FLOWERING LOCUS T

NBT:

New breeding technique

TFL1:

TERMINAL FLOWER 1

References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi Y, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bernier G, Kinet JM, Sachs RM (1981) The physiology of flowering, vol. I: the initiation of flowers. FL CRC Press, Boca Raton

    Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulley SN, Malnoy M, Atkinson RG, Aldwinckle HS (2007) Transformed apples: traits of significance to growers and consumers. Transgenic Plant J 1:267–279

    Google Scholar 

  • Chardon F, Damerval C (2005) Phylogenomic Analysis of the PEBP Gene Family in Cereals. J Mol Evol 61:579–590. doi:10.1007/s00239-004-0179-4

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  CAS  PubMed  Google Scholar 

  • Davies K, Winefield C, Lewis D, Nielsen K, Bradley M, Schwinn K, Deroles S, Manson D, Jordan B (1997) Research into control of flower colour and flowering time in Eustoma grandiflorum (Lisianthus). Flower Newsl 23:24–32

    Google Scholar 

  • Devlin FP, Kay SA (2000) Flower arranging in Arabidopsis. Science 288:1600–1602

    Article  CAS  PubMed  Google Scholar 

  • Gleba Y, Marillonnet S, Klimyuk V (2004) Engineering viral expression vectors for plants: the ‘full virus’ and the ‘deconstructed virus’ strategies. Curr Opin Plant Biol 7:182–188

    Article  CAS  PubMed  Google Scholar 

  • Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 24:7748–7753

    Article  Google Scholar 

  • Harbaugh BK (1995) Flowering of Eustoma grandiflorum (Raf.) Shinn. cultivars influenced by photoperiod and temperature. Hortscience 30:1375–1377

    Google Scholar 

  • Hisamatsu T, Koshika M, Oyama N, Mander LN (1999) The relationship between endogenous gibberellins and rosetting in Eustoma grandiflorum. Jpn Soc Hortic Sci 68:433–527

    Google Scholar 

  • Igarashi A, Yamagata K, Sugai T, Takahashi Y, Sugawara E, Tamura A et al (2009) Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology 386:407–416. doi:10.1016/j.virol.2009.01.039

    Article  CAS  PubMed  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 

  • Ito T, Yoshida K (1997) The etiology of apple russet ring disease. Ann Phytopathol Soc Jpn 63:487

    Google Scholar 

  • Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054

    Article  CAS  PubMed  Google Scholar 

  • Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60:614–625

    Article  CAS  PubMed  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  CAS  PubMed  Google Scholar 

  • Kishigami R, Yamagishi N, Ito T, Yoshikawa N (2014) Detection of apple latent spherical virus in seeds and seedlings from infected apple trees by reverse transcription quantitative PCR and deep sequencing: evidence for lack of transmission of the virus to most progeny seedlings. J Gen Plant Pathol 80:490–498

    Article  CAS  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    Article  CAS  PubMed  Google Scholar 

  • Koganezawa H, Yanase H, Ochiai M, Sakuma T (1985) An isometric virus-like particle isolated from russet ring-diseased apple. Ann Phytopathol Soc Jpn 51:363 (Abstract in Japanese)

    Article  Google Scholar 

  • Kohlein F (1991) Gentians. Timber Press, Portland

    Google Scholar 

  • Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535

    Article  CAS  PubMed  Google Scholar 

  • Kong F, Liu B, Xia Z, Sato S, Kim BM, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, Abe J (2010) Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol 154:1220–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koorneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49:345–370

    Article  Google Scholar 

  • Lazakis CM, Coneva V, Colasanti J (2011) ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J Exp Bot 62:4833–4842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Gall O, Sanfaçon H, Ikegami M, Iwanami T, Jones T, Karasev A, Lehto K, Wellink J, Wetzel T, Yoshikawa N (2007) Cheravirus and Sadwavirus: two unassigned genera of plant positive-sense single-stranded RNA viruses formerly considered atypical members of the genus Nepovirus (family Comoviridae). Arch Virol 152:1767–1774

    Article  PubMed  Google Scholar 

  • Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254

    Article  CAS  PubMed  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant Cell 10:1973–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Gu M, Shi N, Zhang H, Yang N, Osman T, Liu Y, Wang H, Vatish M, Jackson S, Hong Y (2011) Mobile FT mRNA contributes to the systemic florigen signalling in floral induction. Sci Rep 1:73. doi:10.1038/srep00073

    PubMed  PubMed Central  Google Scholar 

  • Li C, Sasaki N, Isogai M, Yoshikawa Y (2004) Stable expression of foreign proteins in herbaceous and apple plants using apple latent spherical virus RNA2 vectors. Arch Virol 149:1541–1558

    CAS  PubMed  Google Scholar 

  • Li C, Yoshikawa N, Takahashi T, Yoshida K, Koganezawa H (2000) Nucleotide sequence and genome organization of Apple latent spherical virus: a new virus classified into the family Comoviridae. J Gen Virol 81:541–547. doi:10.1099/0022-1317-81-2-541

    Article  CAS  PubMed  Google Scholar 

  • Li C, Zhang KE, Zeng X, Jackson S, Zhou Y, Hong Y (2009) A cis element within Flowering locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA. J Virol 83:3540–3548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lifschitz E, Eshed Y (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J Exp Bot 57:3405–3414

    Article  CAS  PubMed  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka KI, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu K-J, Huang N-C, Liu Y-S, Lu C-A, Yu T-S (2012) Long-distance movement of Arabidopsis FLOWERING LOCUS T RNA participates in systemic floral regulation. RNA Biol 9:653–662. doi:10.4161/rna.19965

    Article  CAS  PubMed  Google Scholar 

  • Lusser M, Parisi C, Plan D, Rodríguez-Cerezo E (2011) New plant breeding techniques. State-of-the-art and prospects for commercial development. JRC Technical Report EUR 24760 EN

  • Mathieu J, Warthmann N, Küttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060

    Article  CAS  PubMed  Google Scholar 

  • Matsoukas IG (2014) Attainment of reproductive competence, phase transition, and quantification of juvenility in mutant genetic screens. Front Plant Sci 5:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsoukas IG, Massiah AJ, Thomas B (2012) Florigenic and antiflorigenic signaling in plants. Plant Cell Physiol 53:1827–1842

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137:149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakatsuka T, Haruta KS, Pitaksutheepong C, Abe Y, Kakizaki Y, Yamamoto K, Shimada N, Yamamura S, Nishihara M (2008) Identification and characterization of R2R3-MYB and bHLH transcription factors regulating anthocyanin biosynthesis in gentian flowers. Plant Cell Physiol 49:1818–1829

    Article  CAS  PubMed  Google Scholar 

  • Nakatsuka T, Abe Y, Kakizaki Y, Kubota A, Shimada N, Nishihara M (2009) Over-expression of Arabidopsis FT gene reduces juvenile phase and induces early flowering in ornamental gentian plants. Euphytica 168:113–119

    Article  CAS  Google Scholar 

  • Nakatsuka T, Mishiba K, Kubota A, Abe Y, Yamamura S, Nakamura N, Tanaka Y, Nishihara M (2010) Genetic engineering of novel flower colour by suppression of anthocyanin modification genes in gentian. J Plant Physiol 167:231–237

    Article  CAS  PubMed  Google Scholar 

  • Nakatsuka T, Saito M, Yamada E, Fujita K, Kakizaki Y, Nishihara M (2012) Isolation and characterization of GtMYBP3 and GtMYBP4, orthologues of R2R3-MYB transcription factors that regulate early flavonoid biosynthesis, in gentian flowers. J Exp Bot 63:6505–6517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohkawa K, Kano K, Kanematsu K, Korenaga M (1991) Effects of air temperature and time on rosette formation in seedlings of Eustoma grandiflorum (Raf.) Shinn. Sci Hort 48:171–176. doi:10.1016/0304-4238(91)9016-T

    Article  Google Scholar 

  • Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593

    Article  PubMed  Google Scholar 

  • Purkayastha A, Dasgupta I (2009) Virus-induced gene silencing: a versatile tool for discovery of gene functions in plants. Plant Physiol Biochem 47:967–976

    Article  CAS  PubMed  Google Scholar 

  • Sasaki S, Yamagishi N, Yoshikawa N (2011) Efficient virus-induced gene silencing in apple, pear and Japanese pear using Apple latent spherical virus vectors. Plant Methods 7:15. doi:10.1186/1746-4811-7-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. Bioessays 22:38–47

    Article  CAS  PubMed  Google Scholar 

  • Schiemann J (2014) New plant breeding techniques: prospects for the future. Natural History Museum/nhm.ac.uk

  • Sgamma T, Jackson A, Muleo R, Thomas B, Massiah A (2014) TEMPRANILLO is a regulator of juvenility in plants. Sci Rep 15:4

    Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson GG, Gendall AR, Dean C (1999) When to switch to flowering. Annu Rev Cell Dev Biol 15:519–550

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Jia Z, Cao D, Jiang B, Wu C, Hou W, Liu Y, Fei Z, Zhao D, Han T (2011) GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PLOS One. doi:10.1371/journal.pone.0029238

    Google Scholar 

  • Thomas B, Vince-Prue D (1997) Photoperiodism in plants. Academic Press, San Diego

    Google Scholar 

  • UPOV multimedia (2011) Ashiro Rindo Story http://www.upov.int/multimedia/en/2011/ashiro_rindo.html. Accessed October 9, 2015

  • Van Nocker S, Gardiner SE (2014) Breeding better cultivars, faster: applications of new technologies for the rapid deployment of superior horticultural tree crops. Hortic Res 1:14022

    Article  PubMed  PubMed Central  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yaegashi H, Yamatsuta T, Takahashi T, Li C, Isogai M, Kobori T, Ohki S, Yoshikawa N (2007) Characterization of virus-induced gene silencing in tobacco plants infected with apple latent spherical virus. Arch Virol 152:1839–1849

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi N, Sasaki S, Yamagata K, Komori S, Nagase M, Wada M et al (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. doi:10.1007/s11103-010-9718-0

    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, Yoshikawa N (2010) Highly efficient inoculation method of apple viruses to apple seedlings. Julius Kühn Archiv 427:226

    Google Scholar 

  • Yamagishi N, Kishigami R, Yoshikawa N (2014) Reduced generation time of apple seedlings to within a year by means of a plant virus vector: a new plant-breeding technique with no transmission of genetic modification to the next generation. Plant Biotechnol J 12:60–68

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189

    Article  CAS  PubMed  Google Scholar 

  • Wazir JS (2014) Evaluation of eustoma/lisianthus cultivars for assessing their suitability as prominent new cut flower crop under mid hill conditions of H.P. Int J Agric Sc & Vet Med 2(1):105–110

    Google Scholar 

Download references

Acknowledgments

We are grateful to Mizue Hoshi and Kazumichi Fujiwara (Iwate Agricultural Research Center, 20-1 Narita, Kitakami city, Iwate, 024-0003, Japan) for supplying gentian seeds of cultivar ‘Iwate Yume Aoi’. This study was part of the Cross-ministerial Strategic Innovation Promotion Program ‘Technologies for creating next-generation agriculture, forestry, and fisheries’ supported by the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries, and Food Industry, and by the Council for Science, Technology, and Innovation.

Author information

Authors and Affiliations

  1. Plant Pathology Laboratory, Faculty of Agriculture, Iwate University, Morioka, 020-8550, Japan

    Rym Fekih, Noriko Yamagishi & Nobuyuki Yoshikawa

Authors
  1. Rym Fekih
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noriko Yamagishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nobuyuki Yoshikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nobuyuki Yoshikawa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fekih, R., Yamagishi, N. & Yoshikawa, N. Apple latent spherical virus vector-induced flowering for shortening the juvenile phase in Japanese gentian and lisianthus plants. Planta 244, 203–214 (2016). https://doi.org/10.1007/s00425-016-2498-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2498-2

Keywords

Search

Navigation