Skip to main content
SpringerLink
Log in

Storage temperature controls the timing of garlic bulb formation via shoot apical meristem termination

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

Abstract

Main conclusion

Timing of bulb formation and floral stem induction in garlic is controlled by preplanting storage temperature and shoot apical meristem termination, probably via FLOWERING LOCUS T (FT) genes.

Garlic is planted in the winter, undergoes a vegetative stage, then forms bulbs in response to increasing temperature and lengthening photoperiod. Herein, the storage conditions for propagation bulbs are shown to potentially affect future vegetative-stage length and timing of bulb formation. Storage temperatures of 2 or 33 °C inhibited internal bud growth. Levels of endogenous abscisic acid (ABA) and its inactive isomer trans-ABA were significantly higher in the internal bud of cloves stored at 33 vs. 2 °C, and exogenous ABA treatment before planting confirmed its inhibitory effect on foliage leaf development. Bulb formation started 30 and 60 days after planting of cloves stored at 2 and 33 °C, respectively. Warm storage temperature induced the formation of multiple leaves and cloves after planting. Plants from cloves stored at warm temperature developed a floral stem, whereas those from cold storage did not. Allium sativum FLOWERING LOCUS T1 (AsFT1) was upregulated 2.5- and 4.5-fold in the internal bud and storage leaf, respectively, after 90 and 150 days of cold vs. warm storage. Expression of AsFT4, expected to be antagonist to AsFT1, was 2- to 3-fold lower in the internal bud from cold storage. Expression of AsFT2, associated with floral termination, was 2- to 3- and 10- to 12-fold higher for cold vs. warm storage temperatures, in the internal bud and storage leaf, respectively. Early bulb formation, induced by cold storage, is suggested to inhibit normal foliage leaf development and transition of the shoot apical meristem to reproductive meristem, through regulation of FT genes.

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

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

FT:

FLOWERING LOCUS T

SAM:

Shoot apical meristem

References

  • Abelenda JA, Navarro C, Prat S (2013) Flowering and tuberization: a tale of two nightshades. Trends Plant Sci 19:115–122

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Arguello J, Ledesma A, Bottini R (1991) Hormonal regulation of dormancy in garlic (Allium sativum L.) cv Rosado Paraguayo. Agriscientia 8:9–14

    Google Scholar 

  • Block E (2010) Garlic and other alliums: the lore and the science. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Brewster JL (2008) Onions and other vegetable alliums, 2nd edn. Crop production science in horticulture, vol 15. CABI Publishing, Wallingford

  • Cardellina JH (2013) Review of garlic and other alliums. The lore and the science. J Natural Prod 76:813

    Article  CAS  Google Scholar 

  • Chiwocha SDS, Abrams SR, Ambrose SJ, Cutler AJ, Loewen M, Ross ARS, Kermode AR (2003) A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant J 35:405–417

    Article  CAS  PubMed  Google Scholar 

  • Chiwocha SD, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross AR, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48

    Article  CAS  PubMed  Google Scholar 

  • Chope GA, Cools K, Hammond JP, Thompson AJ, Terry LA (2012) Physiological, biochemical and transcriptional analysis of onion bulbs during storage. Ann Bot 109:819–831

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davies PJ (2010) The plant hormones: Their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones. Biosynthesis, signal transduction, action! 3rd edn. Springer, Dordrecht Heidelberg London New York, pp 1–15

  • Dennis FG Jr (1996) A physiological comparison of seed and bud dormancy. In: Lang GA (ed) Plant dormancy: Physiology, biochemistry and molecular biology. CABI, Wallingford, pp 47–56

    Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Cur Biol 21:R365–R373

    Article  CAS  Google Scholar 

  • Dini C, Fabbri A, Geraci A (2011) The potential role of garlic (Allium sativum) against the multi-drug resistant tuberculosis pandemic: a review. Annali dell’Istituto Superiore di Sanità 47:465–473

    PubMed  Google Scholar 

  • Foley ME (2001) Seed dormancy: an update on terminology, physiological genetics, and quantitative trait loci regulating germinability. Weed Sci 49:305–317

    Article  CAS  Google Scholar 

  • Galiba G, Vágújfalvi A, Li C, Soltész A, Dubcovsky J (2009) Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci 176:12–19

    Article  CAS  Google Scholar 

  • Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35:1769–1786

    Article  CAS  PubMed  Google Scholar 

  • Kamenetsky R (2007) Garlic: botany and horticulture. Hort Rev 33:123

    Article  CAS  Google Scholar 

  • Kamenetsky R, Okubo H (2012) Ornamental geophytes: From basic science to sustainable production. CRC Press, Boca Raton

    Book  Google Scholar 

  • Kamenetsky R, Rabinowitch HD (2001) Floral development in bolting garlic. Sex Plant Reprod 13:235–241

    Article  Google Scholar 

  • Kamenetsky R, Shafir IL, Zemah H, Barzilay A, Rabinowitch H (2004) Environmental control of garlic growth and florogenesis. J Am Soc Hort Sci 129:144–151

    Google Scholar 

  • Kamenetsky R, Faigenboim A, Shemesh Mayer E, Ben Michael T, Gershberg C, Kimhi S, Esquira I, Rohkin Shalom S, Eshel D, Rabinowitch HD, Sherman A (2015) Integrated transcriptome catalogue and organ-specific profiling of gene expression in fertile garlic (Allium sativum L.). BMC Genomics 16:12

  • 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 

  • Kebrom TH, Spielmeyer W, Finnegan EJ (2013) Grasses provide new insights into regulation of shoot branching. Trend Plant Sci 18:41–48

    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 

  • Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105

    Article  CAS  PubMed  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 

  • Krontal Y, Kamenetsky R, Rabinowitch H (2000) Flowering physiology and some vegetative traits of short-day shallot: a comparison with bulb onion. J Hort Sci Biotech 75:35–41

    Google Scholar 

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

    Google Scholar 

  • Lee R, Baldwin S, Kenel F, McCallum J, Macknight R (2013) FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat Comm 4:2884

    Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mann LK (1952) Anatomy of the garlic bulb and factors affecting bulb development. In: California Agricultural Experiment Station, Berkele,y vol. 21, pp 195–251

  • Matsubara S, Kimura I (1991) Changes of ABA content during bulbing and dormancy and in vitro bulbing in onion [Allium cepa] plant. J Jpn Soc Hortic Sci 59:757–762

    Article  CAS  Google Scholar 

  • McCarty DR (1986) A simple method for extraction of RNA from maize tissue. Maize Genet Coop News 60:61

    Google Scholar 

  • Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–122

    Article  CAS  PubMed  Google Scholar 

  • Neta R, David-Schwartz R, Peretz Y, Sela I, Rabinowitch HD, Flaishman M, Kamenetsky R (2011) Flower development in garlic: the ups and downs of gaLFY expression. Planta 233:1063–1072

    Article  CAS  PubMed  Google Scholar 

  • Noy-Porat T, Cohen D, Mathew D, Eshel A, Kamenetsky R, Flaishman MA (2013) Turned on by heat: differential expression of FT and LFY-like genes in Narcissus tazetta during floral transition. J Exp Bot 64:3273–3284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Okubo H, Uemoto S (1981) Changes in the endogenous growth regulators in bulbous iris in bulb-forming and nonbulb-forming aspects. Plant Cell Physiol 22:297–301

    CAS  Google Scholar 

  • Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400

    Article  CAS  PubMed  Google Scholar 

  • Rahim M, Fordham R (1988) Effect of storage temperature on the initiation and development of garlic cloves (Allium sativum L.). Sci Hortic 37:25–38

    Article  Google Scholar 

  • Rahman MH, Haque MS, Karim MA, Ahmed M (2006) Effects of gibberellic acid (GA3) on breaking dormancy in garlic (Allium sativum L.). In J Agri Biol 8:63–65

    CAS  Google Scholar 

  • Samach A, Wigge PA (2005) Ambient temperature perception in plants. Curr Opin Plant Biol 8:483–486

    Article  PubMed  Google Scholar 

  • Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239:27–38

    Article  CAS  PubMed  Google Scholar 

  • Takagi H (1990) Garlic Allium sativum L. In: Rabinowitch H, Brewster J (eds) Onions and allied crops. Biochemistry, food science and minor crops, vol III. CRC Press, Boca Raton, pp 109–146

  • Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Teper-Bamnolker P, Dudai N, Fischer R, Belausov E, Zemach H, Shoseyov O, Eshel D (2010) Mint essential oil can induce or inhibit potato sprouting by differential alteration of apical meristem. Planta 232:179–186

    Article  CAS  PubMed  Google Scholar 

  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

    Article  CAS  PubMed  Google Scholar 

  • Wang C-S, Vodkin LO (1994) Extraction of RNA from tissues containing high levels of procyanidins that bind RNA. Plant Mol Biol Rep 12:132–145

    Article  CAS  Google Scholar 

  • Xue-Xuan X, Hong-Bo S, Yuan-Yuan M, Gang X, Jun-Na S, Dong-Gang G, Cheng-Jiang R (2010) Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abiotic-stressed conditions. Crit Rev Biotechnol 30:222–230

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki H, Nishijima T, Yamato Y, Koshioka M, Miura H (1999) Involvement of abscisic acid (ABA) in bulb dormancy of Allium wakegi Araki I. Endogenous levels of ABA in relation to bulb dormancy and effects of exogenous ABA and fluridone. Plant Growth Regul 29:189–194

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by a grant from the Chief Scientist of the Ministry of Agriculture and Rural Development of Israel (No. 256-0896-12). The manuscript is a contribution of the Agricultural Research Organization, the Volcani Center, Bet Dagan, Israel, No. 694/14.

Author information

Authors and Affiliations

  1. Department of Postharvest Science of Fresh Produce, The Volcani Center, ARO, Bet Dagan, Israel

    Sarit Rohkin Shalom, Yohanan Zutahy, Paula Teper-Bamnolker & Dani Eshel

  2. Robert H. Smith Faculty of Agriculture, Food and Environment, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel

    Sarit Rohkin Shalom

  3. Southern Arava Research and Development Center, Yotvata, Israel

    Daryl Gillett

  4. Department of Fruit Tree Science, The Volcani Center, ARO, Bet Dagan, Israel

    Hanita Zemach

  5. Department of Ornamental Horticulture, The Volcani Center, ARO, Bet Dagan, Israel

    Sagie Kimhi, Itzhak Forer & Rina Kamenetsky

  6. Department of Plant Pathology and Weed Science, The Volcani Center, ARO, Bet Dagan, Israel

    Yehudit Tam

Authors
  1. Sarit Rohkin Shalom
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daryl Gillett
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanita Zemach
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sagie Kimhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Itzhak Forer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yohanan Zutahy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yehudit Tam
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paula Teper-Bamnolker
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rina Kamenetsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dani Eshel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dani Eshel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 83 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rohkin Shalom, S., Gillett, D., Zemach, H. et al. Storage temperature controls the timing of garlic bulb formation via shoot apical meristem termination. Planta 242, 951–962 (2015). https://doi.org/10.1007/s00425-015-2334-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2334-0

Keywords

Search

Navigation