Comparative metabolic profiling of Vitis amurensis and Vitis vinifera during cold acclimation

Fengmei Chai , Wenwen Liu , Yue Xiang , Xianbin Meng , Xiaoming Sun , Cheng Cheng , Guotian Liu , Lixin Duan , Haiping Xin , Shaohua Li

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 8

PDF (1814KB)
Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :8 DOI: 10.1038/s41438-018-0083-5
Article
research-article
Comparative metabolic profiling of Vitis amurensis and Vitis vinifera during cold acclimation
Author information +
History +
PDF (1814KB)

Abstract

Vitis amurensis is a wild Vitis plant that can withstand extreme cold temperatures. However, the accumulation of metabolites during cold acclimation (CA) in V. amurensis remains largely unknown. In this study, plantlets of V. amurensis and V. vinifera cv. Muscat of Hamburg were treated at 4 °C for 24 and 72 h, and changes of metabolites in leaves were detected by gas chromatography coupled with time-of-flight mass spectrometry. Most of the identified metabolites, including carbohydrates, amino acids, and organic acids, accumulated in the two types of grape after CA. Galactinol, raffinose, fructose, mannose, glycine, and ascorbate were continuously induced by cold in V. amurensis, but not in Muscat of Hamburg. Twelve metabolites, including isoleucine, valine, proline, 2-oxoglutarate, and putrescine, increased in V. amurensis during CA. More galactinol, ascorbate, 2-oxoglutarate, and putrescine, accumulated in V. amurensis, but not in Muscat of Hamburg, during CA, which may be responsible for the excellent cold tolerance in V. amurensis. The expression levels of the genes encoding β-amylase (BAMY), galactinol synthase (GolS), and raffinose synthase (RafS) were evaluated by quantitative reverse transcription-PCR. The expression BAMY (VIT_02s0012g00170) and RafS (VIT_05s0077g00840) were primarily responsible for the accumulation of maltose and raffinose, respectively. The accumulation of galactinol was attributed to different members of GolS in the two grapes. In conclusion, these results show the inherent differences in metabolites between V. amurensis and V. vinifera under CA.

Cite this article

Download citation ▾
Fengmei Chai, Wenwen Liu, Yue Xiang, Xianbin Meng, Xiaoming Sun, Cheng Cheng, Guotian Liu, Lixin Duan, Haiping Xin, Shaohua Li. Comparative metabolic profiling of Vitis amurensis and Vitis vinifera during cold acclimation. Horticulture Research, 2019, 6 (1) : 8 DOI:10.1038/s41438-018-0083-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Thomashow, M. F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant. Biol. 50, 571-599 (1999).

[2]

Smallwood, M. & Bowles, D. J. Plants in a cold climate. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 831-847 (2002).

[3]

Thomashow, M. F. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118, 1-7 (1998).

[4]

Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends Plant. Sci. 7, 405-410 (2002).

[5]

Hare, P. D., Cress, W. A. & Staden, J. V. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21, 535-553 (1998).

[6]

Xin, Z. G. & Browse, J. eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl. Acad. Sci. USA 95, 7799-7804 (1998).

[7]

Wanner, L. A. & Junttila, O. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120, 391-399 (1999).

[8]

Dorffling, K. et al. Heritable improvement of frost tolerance in winter wheat by in vitro-selection of hydroxyproline-resistant proline overproducing mutants. Euphytica 93, 1-10 (1997).

[9]

Janska, A., Marsik, P., Zelenkova, S. & Ovesna, J . Cold stress and acclimation - what is important for metabolic adjustment?. Plant Biol. 12, 395-405 (2010).

[10]

Shulaev, V., Cortes, D., Miller, G. & Mittler, R. Metabolomics for plant stress response. Physiol. Plant. 132, 199-208 (2008).

[11]

Weckwerth, W. & Fiehn, O. Can we discover novel pathways using metabolomic analysis?. Curr. Opin. Biotech. 13, 156-160 (2002).

[12]

Morgenthal, K., Weckwerth, W. & Steuer, R. Metabolomic networks in plants: transitions from pattern recognition to biological interpretation. Bio. Syst. 83, 108-117 (2006).

[13]

Barding, G. A., Beni, S., Fukao, T., Bailey-Serres, J. & Larive, C. K. Comparison of GC-MS and NMR for metabolite profiling of rice subjected to submergence stress. J. Proteome Res. 12, 898-909 (2013).

[14]

Wen, Y. Q. et al. Using the combined analysis of transcripts and metabolites to propose key genes for differential terpene accumulation across two regions. BMC Plant Biol. 15, 240 (2015).

[15]

Dunn, W. B. et al. Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat. Protoc. 6, 1060-1083 (2011).

[16]

Takahashi, H., Morimoto, T., Ogasawara, N. & Kanaya, S. AMDORAP: non-targeted metabolic profiling based on high-resolution LC-MS. BMC Bioinform. 12, 259 (2011).

[17]

Barding, G. A. Jr., Fukao, T., Beni, S., Bailey-Serres, J. & Larive, C. K. Differential metabolic regulation governed by the rice SUB1A gene during submergence stress and identification of alanylglycine by 1H NMR spectroscopy. J. Proteome Res. 11, 320-330 (2012).

[18]

Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A. R. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396 (2006).

[19]

Cook, D., Fowler, S., Fiehn, O. & Thomashow, M. F. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. USA 101, 15243-15248 (2004).

[20]

Hannah, M. A. et al. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol. 142, 98-112 (2006).

[21]

Maruyama, K. et al. Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiol. 164, 1759-1771 (2014).

[22]

Morsy, M. R., Jouve, L., Hausman, J. F., Hoffmann, L. & Stewart, J. M. Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J. Plant. Physiol. 164, 157-167 (2007).

[23]

Juhasz, Z. et al. Pleiotropic effect of chromosome 5A and the mvp mutation on the metabolite profile during cold acclimation and the vegetative/generative transition in wheat. BMC Plant Biol. 15, 57 (2015).

[24]

Davik, J. et al. Dehydrin, alcohol dehydrogenase, and central metabolite levels are associated with cold tolerance in diploid strawberry (Fragaria spp.). Planta 237, 265-277 (2013).

[25]

Lee, Y. P. et al. Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella sp. and Arabidopsis thaliana accessions. BMC Plant Biol. 12, 131 (2012).

[26]

Benina, M. et al. Comparative metabolic profiling of Haberlea rhodopensis, Thellungiella halophyla, and Arabidopsis thaliana exposed to low temperature. Front. Plant Sci. 4, 499 (2013).

[27]

Zuther, E., Schulz, E., Childs, L. H. & Hincha, D. K. Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ. 35, 1860-1878 (2012).

[28]

Gray, G. R. & Heath, D. A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting. Physiol. Plant. 124, 236-248 (2005).

[29]

Kaplan, F. et al. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136, 4159-4168 (2004).

[30]

Rohde, P., Hincha, D. K. & Heyer, A. G. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J. 38, 790-799 (2004).

[31]

Krasensky, J. & Jonak, C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593-1608 (2012).

[32]

Vivier, M. A. & Pretorius, I. S. Genetically tailored grapevines for the wine industry. Trends Biotechnol. 20, 472-478 (2002).

[33]

Xin, H. et al. Genome wide transcriptional profile analysis of Vitis amurensis and Vitis vinifera in response to cold stress. PLoS. One. 8, e58740 (2013).

[34]

Fennell, A. Freezing tolerance and injury in grapevines. J. Crop Improv. 10, 201-235 (2004).

[35]

Wan, Y. et al. The eco-geographic distribution of wild grape germplasm in China. VITIS 47, 77-80 (2008).

[36]

Xu, W. et al. Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress. Plant Mol. Biol. 86, 527-541 (2014).

[37]

Li, J., Wang, N., Xin, H. & Li, S. Overexpression of VaCBF4, a transcription factor from Vitis amurensis, improves cold tolerance accompanying increased resistance to drought and salinity in Arabidopsis. Plant. Mol. Biol. Rep. 31, 1518-1528 (2013).

[38]

Li, J. et al. Characterization of two VvICE1 genes isolated from ‘Muscat Hamburg’ grapevine and their effect on the tolerance to abiotic stresses. Sci. Hortic.-Amst. 165, 266-273 (2014).

[39]

Sun, X. et al. Ethylene positively regulates cold tolerance in grapevine by modulating the expression of ETHYLENE RESPONSE FACTOR 057. Sci. Rep. 6, 24066 (2016).

[40]

Yuan, Y. et al. Overexpression of VaPAT1, a GRAS transcription factor from Vitis amurensis, confers abiotic stress tolerance in Arabidopsis. Plant Cell Rep. 35, 655-666 (2016).

[41]

Weckwerth, W., Wenzel, K. & Fiehn, O. Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4, 78-83 (2004).

[42]

Fernie, A. R. et al. Recommendations for reporting metabolite data. Plant Cell 23, 2477-2482 (2011).

[43]

Guo, R. et al. Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol. 15, 170 (2015).

[44]

Wagner, C., Sefkow, M. & Kopka, J. Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry 62, 887-900 (2003).

[45]

Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, 279-285 (2016).

[46]

Marchler-Bauer, A. et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 45, D200-D203 (2016).

[47]

Sun, X. et al. The GARP/MYB-related grape transcription factor AQUILO improves cold tolerance and promotes the accumulation of raffinose family oligosaccharides. J. Exp. Bot. 69, 1749-1764 (2018).

[48]

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

[49]

ElSayed, A. I., Rafudeen, M. S. & Golldack, D. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol. 16, 1-8 (2014).

[50]

Kaplan, F. & Guy, C. L. β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 135, 1674-1684 (2004).

[51]

Klotke, J., Kopka, J., Gatzke, N. & Heyer, A. G. Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation - evidence for a role of raffinose in cold acclimation. Plant Cell Environ. 27, 1395-1404 (2004).

[52]

Hameed, A., Iqbal, N. & Malik, S. A. Mannose-induced modulations in antioxidants, protease activity, lipid peroxidation, and total phenolics in etiolated wheat leaves. J. Plant. Growth Regul. 28, 58-65 (2009).

[53]

Hameed, A., Iqbal, N. & Malik, S. A. Effect of d-mannose on antioxidant defense and oxidative processes in etiolated wheat coleoptiles. Acta Physiol. Plant. 36, 161-167 (2013).

[54]

Goto, S. et al. Organizing and computing metabolic pathway data in terms of binary relations. Pacific Symposium Biocomput. 1997, 175-186 (1997).

[55]

Hoffman, L., DaCosta, M., Ebdon, J. S. & Watkins, E. Physiological changes during cold acclimation of perennial ryegrass accessions differing in freeze tolerance. Crop Sci. 50, 1037-1047 (2010).

[56]

Conklin, P. L. Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ. 24, 383-394 (2001).

[57]

Shelden, M. C., Dias, D. A., Jayasinghe, N. S., Bacic, A. & Roessner, U. Root spatial metabolite profiling of two genotypes of barley (Hordeum vulgare L.) reveals differences in response to short-term salt stress. J. Exp. Bot. 67, 3731-3745 (2016).

[58]

Capell, T., Bassie, L. & Christou, P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl. Acad. Sci. USA 101, 9909-9914 (2004).

[59]

Rohloff, J. et al. Metabolite profiling reveals novel multi-level cold responses in the diploid model Fragaria vesca (woodland strawberry). Phytochemistry 77, 99-109 (2012).

[60]

Kim, T. E., Kim, S. K., Han, T. J., Lee, J. S. & Chang, S. C. ABA and polyamines act independently in primary leaves of cold-stressed tomato (Lycopersicon esculentum). Physiol. Plant. 115, 370-376 (2002).

[61]

Urano, K. et al. Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Bioph Res Co. 313, 369-375 (2004).

[62]

Obata, T. & Fernie, A. R. The use of metabolomics to dissect plant responses to abiotic stresses. Cell. Mol. Life Sci. 69, 3225-3243 (2012).

[63]

Joshi, V., Joung, J. G., Fei, Z. & Jander, G. Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39, 933-947 (2010).

[64]

Hayat, S. et al. Role of proline under changing environments. Plant Signal. Behav. 7, 1456-1466 (2012).

[65]

Maruyama, K. et al. Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150, 1972-1980 (2009).

PDF (1814KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/