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Sucrose signaling function on the formation and swelling of bulblets of Lilium sargentiae E.H. Wilson

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Abstract

Lilium sargentiae E.H. Wilson (Liliaceae) is an ornamental and economic flowering bulb in China. Unfortunately, due to low natural bulb multiplication rates or long juvenile phases, commercial release of a new genotype may take 10 or even 20 years. In this study, bulbs were expanded in test tubes by adding sucrose, to shorten the duration of the commercial production cycle. Results indicated that when sucrose, with a concentration of 60 g l−1, was supplied to the culture medium, the bulblets could be most effectively induced and expanded. The effect of sucrose on the formation and expansion of L. sargentiae was obvious and dominant. It was not connected to the osmotic potential of sucrose, nor entirely explained by the function of sucrose as an energy and carbon source. We used sugar analogues in the culturing of explanted materials to research the effect of sucrose-specific signaling on bulblet formation and expansion. Results showed that exogenous 3-O-methyl glucose could not induce and expand test-tube bulblets, which was similar to mannose, whereas isomaltulose could generate similar results to those obtained with sucrose. The results further indicated that the specific signalling of sucrose could be responsible for the effect on bulblets formation and swelling. We used the exclusion method to confirm above results and hypothesis, and observed that only a small part of sucrose was transformed by cell wall invertase and entered the cells through hexose transporters, playing a certain effect on bulbelt growth and development through hexose or hexose signaling systems. Overall, the effect of sucrose on bulblet induction and swelling could be explained by sucrose-specific signaling. Furthermore, this effect has a direct correlation with the sucrose-specific vector.

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References

  • Barratt DH, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ, Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 106:13124–13129

    Article  CAS  PubMed  Google Scholar 

  • Benschop M, Kamenetsky R, Nard ML, Okubo H, Hertogh AD (2010) The global flower bulb industry: production, utilization, research. Hortic Rev 36:1–115

    Google Scholar 

  • Chiou TJ, Bush DR (1998) Sucrose is a signaling molecule in assimilate partitioning. Proc Natl Acad Sci USA 95:4784–4788

    Article  CAS  PubMed  Google Scholar 

  • Cortès S, Gromova M, Evrard A, Roby C, Heyraud A, Rolin DB, Raymond P, Brouquisse RM (2003) In plants, 3-o-methylglucose is phosphorylated by hexokinase but not perceived as a sugar. Plant Physiol 131:824–837

    PubMed  PubMed Central  Google Scholar 

  • Cui HM (2007) Experimental course on plant physiology. Xinjiang University Press, Urumchi, pp 75–76

    Google Scholar 

  • ECFRPS (1980) Flora Reipublicae Popularis Sinicae, vol 14. Science Press, Beijing

    Google Scholar 

  • Greenway H, Munns R, Gibbs J (1982) Effects of accumulation of 3-O-methylglucose on levels of endogenous osmotic solutes in Chlorella emersonii. Plant Cell Environ 5:405–412

    Article  CAS  Google Scholar 

  • Grennan AK, Gragg J (2009) How sweet it is: identification of vacuolar sucrose transporters. Plant Physiol 150:1109–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iraqi D, Le VQ, Lamhamedi MS, Tremblay FM (2005) Sucrose utilization during somatic embryo development in black spruce: involvement of apoplastic invertase in the tissue and of extracellular invertase in the medium. J Plant Physiol 162:115–124

    Article  CAS  PubMed  Google Scholar 

  • Jérémy L, Bertrand L, Marie-Pascale P, Annette MB (2010) Hexokinase-dependent sugar signaling represses fructan exohydrolase activity in Lolium perenne. Funct Plant Biol 37:1151–1160

    Article  CAS  Google Scholar 

  • Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J, Moore BD (2008) Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228:411–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klerk GJ (2012) Micropropagation of bulbous crops: technology and present state. Floric Ornam Biotechnol 6:1–8

    Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540

    Article  CAS  PubMed  Google Scholar 

  • Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11:707–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YF, Ming J, Wang LG, Yuan SX, Liu C, Wang Y, Liang Y, Feng HY, Xu LF (2012) Research progress on basic nutritional and bioactive substances of lily. China Veg 24:7–13

    Google Scholar 

  • Li XY, Wang CX, Cheng JY, Zhang J, Jaime AT, Liu XY, Duan X, Li TL, Sun HM (2014) Transcriptome analysis of carbohydrate metabolism during bulblet formation and development in Lilium davidii var. unicolor. BMC Plant Biol 14:358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malla SB (1994) Medicinal herbs in the Bagamati zone. ICIMOD, Kathmandu, pp 8–28

    Google Scholar 

  • Martínez MT, Vieitez AM, Corredoira E (2015) Improved secondary embryo production in Quercus alba and Q. rubra by activated charcoal, silver thiosulphate and sucrose: influence of embryogenic explant used for subculture. Plant Cell Tissue Organ Cult 121:531–546

    Article  CAS  Google Scholar 

  • Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible WR, Stitt M (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49:463–491

    Article  CAS  PubMed  Google Scholar 

  • Parfitt D, Herbert RJ, Rogers HJ, Francis D (2004) Differential expression of putative floral genes in Pharbitis nil shoot apices cultured on glucose compared with sucrose. J Exp Bot 55:2169–2177

    Article  CAS  PubMed  Google Scholar 

  • Qian JL, Zhu XD, Tian SQ (2004) The preliminary study on growth and cold treatment of test-tube bulblet of ‘Sorbonne’. Acta Hortic Sinica 31:828–828

    Google Scholar 

  • Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Rook F, Gerrits N, Kortstee A, Van KM, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose specific signaling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J Cell Mol Biol 15:253–263

    Article  CAS  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418

    Article  CAS  PubMed  Google Scholar 

  • Sinha AK, Hofmann MG, Römer U, Köckenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128:1480–1489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smeekens S, Rook F (1997) Sugar sensing and sugar mediated signal transduction in plants. Plant Physiol 115:7–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 sucrose/H+ symporter by tissue specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148:200–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeda S, Mano S, Ohto M, Nakamura K (1994) Inhibitors of protein phosphatases 1 and 2A block the sugar-inducible gene expression in plants. Plant Physiol 106:567–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng JB, Wan DG, Cai Y, Zhu YL (2012) Dynamic study of sucrose synthase activity of dendrobium dendrobium. J Chin Med Mater 35:369–371

    CAS  Google Scholar 

  • Turgen R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221

    Article  CAS  Google Scholar 

  • Wang AQ, Zhou QW, He LF, Xu HY, Yang MC (1998) Studies on the bulblet formation in tube of lilium longiflorum L. J Guangxi Agric Univ 17:71–75

    CAS  Google Scholar 

  • Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2003) Activities of enzymes involved in sucrose-to-starch metabolism in rice grains subjected to water stress during filling. Field Crops Res 81:69–81

    Article  Google Scholar 

  • Yang Z, Zhang L, Diao F, Huang M, Wu N (2004) Sucrose regulates elongation of carrot somatic embryo radicles as a signal molecule. Plant Mol Biol 54:441–459

    Article  CAS  PubMed  Google Scholar 

  • Zeng ZD (2014) The four different explants’ tissue culture of Lilium sargentiae. MAgr Thesis. Sichuan Agricultural University, Chengdu

  • Zhang ZL, Li XF (2009) Experimental guidance on plant physiology. Higher Education Press, Beijing

    Google Scholar 

  • Zhang J, Cai XM, Lin Z (2010a) Formation and enlargement of lily bulblet in test tube. Fujian J Agric Sci 25:328–331

    CAS  Google Scholar 

  • Zhang YL, Zhang QX, Xue XN (2010b) The effects of the photoperiods on the bulblet formation and sugar metabolism change of wild lilium lancifolium in vitro. Acta Hortic Sinica 37:957–962

    CAS  Google Scholar 

  • Zhang J, Gai MZ, Xue BY, Jia NN, Wang CX, Wang JX, Sun HM (2017) The use of miRNAs as reference genes for miRNA expression normalization during Lilium somatic embryogenesis by real-time reverse transcription PCR analysis. Plant Cell Tissue Organ Cult 129:105–118

    Article  CAS  Google Scholar 

  • Zhu XD, Tian SQ, Chu HX (2005) Studies on growth and cold treatment of test-tube bulblet of Lilium. Jiangsu Agric Sci 33:74–76

    Google Scholar 

Download references

Acknowledgements

This work was supported by Breeding Project of Sichuan Province 13th Five-Year Plan Tackle Key Problems, China (No. 2016NYZ0038).

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Authors and Affiliations

  1. Garden Research Institute, Sichuan Agricultural University, Huimin Road No.211, Wenjiang District, Chengdu, 611130, Sichuan, China

    Suping Gao, Yuan Zhu, Qibing Chen, Xiaofang Yu, Wenji Li, Ju Hu, Di Hu & Wenhui Si

  2. Provincial Laboratory of Landscape Flower Engineering, Sichuan Agricultural University, Chengdu, 611130, Sichuan, China

    Suping Gao, Ting Lei, Qibing Chen & Xiaofang Yu

  3. Luzhou City Afforestation Administrative Office, Luzhou, 646000, Sichuan, China

    Lingyun Zhou

  4. Triticeae Research Institute, Sichuan Agricultural University, Chengdu, 611130, Sichuan, China

    Yonghong Zhou

  5. Forestry College, Guangxi University, Nanning, 530004, Guangxi, China

    Xiaofeng Fu

Authors
  1. Suping Gao
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  2. Yuan Zhu
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  3. Lingyun Zhou
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  4. Xiaofeng Fu
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  5. Ting Lei
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  7. Xiaofang Yu
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  8. Yonghong Zhou
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  9. Wenji Li
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  10. Ju Hu
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  11. Di Hu
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  12. Wenhui Si
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Contributions

Yuan Zhu and Suping Gao wrote the manuscript. Lingyun Zhou and Yuan Zhu performed experiments. Xiaofeng Fu and Ting Lei assisted with experiments design. Qibing Chen, Xiao Fang Yu and Yonghong Zhou helped to improve the manuscript. Di Hu and Wenji Li analyzed sequencing data and developed analysis tools. Ju Hu and Wenhui Si assisted with analyse experimental results.

Corresponding author

Correspondence to Suping Gao.

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The authors declare that they do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Ethical standards

The experiments were performed according to the current laws of China.

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Communicated by Sergio J. Ochatt.

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Gao, S., Zhu, Y., Zhou, L. et al. Sucrose signaling function on the formation and swelling of bulblets of Lilium sargentiae E.H. Wilson. Plant Cell Tiss Organ Cult 135, 143–153 (2018). https://doi.org/10.1007/s11240-018-1451-4

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  • DOI: https://doi.org/10.1007/s11240-018-1451-4

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