Skip to main content
Log in

Application of galactinol to tomato enhances tolerance to cold and heat stresses

  • Research Report
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

Galactinol, a galactosyl donor, is the key substrate in raffinose family oligosaccharide (RFO) biosynthesis pathways. Many studies proved that galactinol also regulates some defense-related genes to be transcribed as a sugar signal under biotic and abiotic stresses. There are four galactinol synthase (SlGolS) genes in tomato. In this study, SlGolS1, SlGolS2, and SlGolS4 responded to cold stress, especially SlGolS1 stems treated for 12 h and SlGolS4 stems treated for 24 h. Under heat stress, the expression levels of SlGolS1, SlGolS2, and SlGolS3, especially SlGolS1 and SlGolS2, increased in leaves, roots, and stems. When expressed in E. coli cells, SlGolS2 and SlGolS4 enhanced cold tolerance, whereas SlGolS1 and SlGolS3 improved heat tolerance. These results suggested that SlGolS family members played different roles in tolerance to cold and heat stresses. In addition, the application of galactinol or galactinol + α-galactosidase inhibitor (DGJ) improved the cold and heat tolerances of tomato plants, whereas the single application of DGJ had no effect. Interestingly, the applications of DGJ, galactinol, and galactinol + DGJ also affected the expression levels of SlRS, SlSTS, and SlAGAL under cold and heat stresses. These findings indicated that galactinol was involved in the biosynthesis pathways of RFOs as a galactosyl donor and regulated the expression levels of RFO biosynthesis and breakdown-related genes as a sugar signal under cold and heat stresses.

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

Data availability

All data in this study are available from the corresponding author on reasonable request.

References

  • Bhattacharya S, Kundu A (2020) Sugars and sugar polyols in overcoming environmental stresses. Protective Chemical Agents in the Amelioration of Plant Abiotic Stress, pp 71–101

  • Cui LH, Byun MY, Oh HG, Kim SJ, Lee J, Park H, Lee H, Kim WT (2020) Poaceae type II galactinol synthase 2 from antarctic flowering plant deschampsia antarctica and rice improves cold and drought tolerance by accumulation of raffinose family oligosaccharides in transgenic rice plants. Plant Cell Physiol 61:88–104

    Article  CAS  Google Scholar 

  • de Souza Vidigal D, Willems L, van Arkel J, Dekkers BJW, Hilhorst HWM, Bentsink L (2016) Galactinol as marker for seed longevity. Plant Sci 246:112–118

  • Downie B, Gurusinghe S, Dahal P, Thacker RR, Snyder JC, Nonogaki H, Yim K, Fukanaga K, Alvarado V, Bradford KJ (2003) Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131:1347–1359

    Article  CAS  Google Scholar 

  • ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol (stuttg) 16:1–8

    Article  CAS  Google Scholar 

  • Filiz E, Ozyigit II, Vatansever R (2015) Genome-wide identification of galactinol synthase (GolS) genes in Solanum lycopersicum and Brachypodium distachyon. Comput Biol Chem 58:149–157

    Article  CAS  Google Scholar 

  • Gu L, Han Z, Zhang L, Downie B, Zhao T (2013) Functional analysis of the 5’ regulatory region of the maize GALACTINOL SYNTHASE2 gene. Plant Sci 213:38–45

    Article  CAS  Google Scholar 

  • Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim ZG (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta 203:460–469

    Article  CAS  Google Scholar 

  • Jang JH, Shang Y, Kang HK, Kim SY, Kim BH, Nam KH (2018) Arabidopsis galactinol synthases 1 (AtGOLS1) negatively regulates seed germination. Plant Sci 267:94–101

    Article  CAS  Google Scholar 

  • Jariteh M, Ebrahimzadeh H, Niknam V (2015) Developmental changes of protein, proline and some antioxidant enzymes activities in somatic and zygotic embryosof Persian walnut (Juglans regia L.). Plant Cell Tissue Organ Cult 122:101–115

  • Kim MS, Cho SM, Kang EY, Im YJ, Hwangbo H, Kim YC, Ryu CM, Yang KY, Chung GC, Cho BH (2008) Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol Plant Microbe Interact 21:1643–1653

    Article  CAS  Google Scholar 

  • Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasjarvi J, Mittler R (2019) Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci 24:25–37

    Article  CAS  Google Scholar 

  • Lehle L, Tanne W (1973) The function of myo-inositol in the biosynthesis of raffinose. Purification and characterization of galactinol: sucrose 6-galactosyltransferase from Vicia faba seeds. Eur J Biochem 38:103–110

  • Li T, Zhang Y, Liu Y, Li X, Hao G, Han Q, Dirk LMA, Downie AB, Ruan YL, Wang J, Wang G, Zhao T (2020) Raffinose synthase enhances drought tolerance through raffinose synthesis or galactinol hydrolysis in maize and Arabidopsis plants. J Biol Chem 295:8064–8077

  • Liu YD, Zhang L, Meng SD, Liu YF, Zhao XM, Pan CP, Zhang HD, Xu T, He Y, Qi MF, Li TL (2020) Expression of galactinol synthase from Ammopiptanthus nanus in tomato improves tolerance to cold stress. J Exp Bot 71:435–449

    Article  CAS  Google Scholar 

  • Lu J, Sui X, Ma S, Li X, Liu H, Zhang Z (2017) Suppression of cucumber stachyose synthase gene (CsSTS) inhibits phloem loading and reduces low temperature stress tolerance. Plant Mol Biol 95:1–15

    Article  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  Google Scholar 

  • Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1:1559–1582

    Article  CAS  Google Scholar 

  • Peixoto JV, Neto CM, Campos LF, Dourado WS, Nogueira AP, Nascimento AD (2017) Industrial tomato lines: morphological properties and productivity. Genet Mol Res 16:gmr16029540

  • Pommerrenig B, Ludewig F, Cvetkovic J, Trentmann O, Klemens PAW, Neuhaus HE (2018) In concert: orchestrated changes in carbohydrate homeostasis are critical for plant abiotic stress tolerance. Plant Cell Physiol 59:1290–1299

  • Qiu S, Zhang J, He J, Sha W, Li M, Zhao Y, Zhai Y (2020) Overexpression of GmGolS2–1, a soybean galactinol synthase gene, enhances transgenic tobacco drought tolerance. Plant Cell Tissue Organ Cult (PCTOC) 143:507–516

  • Saito M, Yoshida M (2011) Expression analysis of the gene family associated with raffinose accumulation in rice seedlings under cold stress. J Plant Physiol 168:2268–2271

    Article  CAS  Google Scholar 

  • Salvi P, Kamble NU, Majee M (2018) Stress-inducible galactinol synthase of chickpea (CaGolS) is implicated in heat and oxidative stress tolerance through reducing stress-induced excessive reactive oxygen species accumulation. Plant Cell Physiol 59:155–166

    Article  CAS  Google Scholar 

  • Salvi P, Kamble NU, Majee M (2020) Ectopic over-expression of ABA-responsive chickpea galactinol synthase (CaGolS) gene results in improved tolerance to dehydration stress by modulating ROS scavenging. Environ Exp Bot 171:103957

  • Saravitz D, Pharr D, Carter T (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiol 83:185–189

    Article  CAS  Google Scholar 

  • Selvaraj MG, Ishizaki T, Valencia M, Ogawa S, Dedicova B, Ogata T, Yoshiwara K, Maruyama K, Kusano M, Saito K, Takahashi F, Shinozaki K, Nakashima K, Ishitani M (2017) Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field. Plant Biotechnol J 15:1465–1477

    Article  CAS  Google Scholar 

  • Sengupta S, Mukherjee S, Basak P, Majumder AL (2015) Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci 6:656

    Article  Google Scholar 

  • Shen Y, Jia B, Wang J, Cai X, Hu B, Wang Y, Chen Y, Sun M, Sun X (2020) Functional analysis of Arabidopsis thaliana galactinol synthase AtGolS2 in response to abiotic stress. Mol Plant Breed 11:1–11

    Google Scholar 

  • Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115:1211–1219

    Article  CAS  Google Scholar 

  • Shigeoka S, Onishi T, Nakano Y, Kitaoka S (1987) Characterization and physiological function of glutathione reductase in Euglena gracilis Z. Biochem J 242:511–515

    Article  CAS  Google Scholar 

  • Stengel F, Baldwin AJ, Painter AJ, Jaya N, Basha E, Kay LE, Vierling E, Robinson CV, Benesch JLP (2010) Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. PNAS 107:2007–2012

    Article  CAS  Google Scholar 

  • Strand Å, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2010) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ 26:523–535

  • Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89

    Article  CAS  Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

    Article  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchishinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  Google Scholar 

  • Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    Article  CAS  Google Scholar 

  • Ueda T, Coseo MP, Harrell TJ, Obendorf RL (2005) A multifunctional galactinol synthase catalyzes the synthesis of fagopyritol a1 and fagopyritol b1 in buckwheat seed. Plant Sci 168:681–690

    Article  CAS  Google Scholar 

  • Valluru R, Van den Ende W (2011) Myo-inositol and beyond–emerging networks under stress. Plant Sci 181:387–400

    Article  CAS  Google Scholar 

  • Vinson CC, Mota APZ, Porto BN, Oliveira TN, Sampaio I, Lacerda AL, Danchin EGJ, Guimaraes PM, Williams TCR, Brasileiro ACM (2020) Characterization of raffinose metabolism genes uncovers a wild Arachis galactinol synthase conferring tolerance to abiotic stresses. Sci Rep 10:15258

  • Wang X, Zhao C, Müller C, Wang C, Ciais P, Janssens IA, Peñuelas J, Asseng S, Li T, Elliott JW, Huang Y, Li L, Piao S (2020) Emergent constraint on crop yield response to warmer temperature from field experiments. Nat Sustain 3:908–916

    Article  Google Scholar 

  • Wheelera TR, Craufurd PQ, Ellis RH, Porter JR, Vara Prasad PV (2000) Temperature variability and the yield of annual crops. Agr Ecosyst Environ 82:159–167

    Article  Google Scholar 

  • Zhang Q, Song X, Bartels D (2018) Sugar metabolism in the desiccation tolerant grass Oropetium thomaeum in response to environmental stresses. Plant Sci 270:30–36

    Article  CAS  Google Scholar 

  • Zhao TY, Meeley RB, Downie B (2003) Aberrant processing of a maize GALACTINOL SYNTHASE transcript is caused by heat stress. Plant Sci 165:245–256

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2019YFD1001902), and National Natural Science Foundation of China (Grant No. 31772295, U1708232).

Author information

Authors and Affiliations

Authors

Contributions

YL and MQ designed the total experiments. YL and ZL planned, conducted and analyzed the gene expression data. JM, SM, and CP finished the application of galactinol and DGJ assays. XZ, HZ, and SW conducted physiological experiments. TX and YH finished the analysis of SlGolS genes in E. coli. YL wrote the manuscript, and all the authors checked it.

Corresponding authors

Correspondence to Yufeng Liu or Mingfang Qi.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Sung-Chur Sim.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Zhang, L., Ma, J. et al. Application of galactinol to tomato enhances tolerance to cold and heat stresses. Hortic. Environ. Biotechnol. 63, 311–323 (2022). https://doi.org/10.1007/s13580-021-00402-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-021-00402-6

Keywords

Navigation