Integrated proteomic and metabolomic analyses reveal the importance of aroma precursor accumulation and storage in methyl jasmonate-primed tea leaves

Jiang Shi , Jiatong Wang , Haipeng Lv , Qunhua Peng , Monika Schreiner , Susanne Baldermann , Zhi Lin

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 95

PDF (2491KB)
Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :95 DOI: 10.1038/s41438-021-00528-9
Article
research-article
Integrated proteomic and metabolomic analyses reveal the importance of aroma precursor accumulation and storage in methyl jasmonate-primed tea leaves
Author information +
History +
PDF (2491KB)

Abstract

In response to preharvest priming with exogenous methyl jasmonate (MeJA), tea plants adjust their physiological behavior at the molecular level. The whole-organism reconfiguration of aroma formation from the precursor to storage is poorly understood. In this study, we performed iTRAQ proteomic analysis and identified 337, 246, and 413 differentially expressed proteins in tea leaves primed with MeJA for 12 h, 24 h, and 48 h, respectively. Furthermore, a total of 266 nonvolatile and 100 volatile differential metabolites were identified by utilizing MS-based metabolomics. A novel approach that incorporated the integration of extended self-organizing map-based dimensionality was applied. The vivid time-scale changes tracing physiological responses in MeJA-primed tea leaves are marked in these maps. Jasmonates responded quickly to the activation of the jasmonic acid pathway in tea leaves, while hydroxyl and glycosyl jasmonates were biosynthesized simultaneously on a massive scale to compensate for the exhausted defense. The levels of α-linolenic acid, geranyl diphosphate, farnesyl diphosphate, geranylgeranyl diphosphate, and phenylalanine, which are crucial aroma precursors, were found to be significantly changed in MeJA-primed tea leaves. Green leaf volatiles, volatile terpenoids, and volatile phenylpropanoids/benzenoids were spontaneously biosynthesized from responding precursors and subsequently converted to their corresponding glycosidic forms, which can be stably stored in tea leaves. This study elucidated the physiological response of tea leaves primed with exogenous methyl jasmonate and revealed the molecular basis of source and sink changes on tea aroma biosynthesis and catabolism in response to exogenous stimuli. The results significantly enhance our comprehensive understanding of tea plant responses to exogenous treatment and will lead to the development of promising biotechnologies to improve fresh tea leaf quality.

Cite this article

Download citation ▾
Jiang Shi, Jiatong Wang, Haipeng Lv, Qunhua Peng, Monika Schreiner, Susanne Baldermann, Zhi Lin. Integrated proteomic and metabolomic analyses reveal the importance of aroma precursor accumulation and storage in methyl jasmonate-primed tea leaves. Horticulture Research, 2021, 8 (1) : 95 DOI:10.1038/s41438-021-00528-9

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Liechti, R. & Farmer, E. The jasmonate pathway. Science 296, 1649-1650 (2002).

[2]

Pauwels, L., Inzé, D. & Goossens, A. Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14, 87-91 (2009).

[3]

Jang, G. et al. Volatile methyl jasmonate is a transmissible form of jasmonate and its biosynthesis is involved in systemic jasmonate response in wounding. Plant Biotechnol. Rep. 8, 409-419 (2014).

[4]

Ziosi, V. et al. Jasmonate-induced transcriptional changes suggest a negative interference with the ripening syndrome in peach fruit. J. Exp. Bot. 59, 563-573 (2008).

[5]

Moreno, F., Blanch, G. P. & Castillo, M. Effect of (-) and (+)-methyl jasmonate on the bioformation of aroma-active esters in strawberry fruits. Eur. Food Res. Technol. 231, 829-834 (2010).

[6]

Cao, S., Cai, Y., Yang, Z. & Zheng, Y. MeJA induces chilling tolerance in loquat fruit by regulating proline and γ-aminobutyric acid contents. Food Chem. 133, 1466-1470 (2012).

[7]

Misra, R. C., Maiti, P., Chanotiya, C. S., Shanker, K. & Ghosh, S. Methyl jasmonate-elicited transcriptional responses and pentacyclic triterpene biosynthesis in sweet basil. Plant Physiol. 164, 1028-1044 (2014).

[8]

Zhang, X., Sheng, J., Li, F., Meng, D. & Shen, L. Methyl jasmonate alters arginine catabolism and improves postharvest chilling tolerance in cherry tomato fruit. Postharvest Biol. Tec. 64, 160-167 (2012).

[9]

Lackman, P. et al. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc. Natl Acad. Sci. USA 108, 5891-5896 (2011).

[10]

Kim, E. et al. Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol. 149, 1751-1760 (2009).

[11]

Peremarti, A. et al. Transcriptional regulation of the rice arginine decarboxylase (Adc1) and S-adenosylmethionine decarboxylase (Samdc) genes by methyl jasmonate. Plant Physiol. Bioch 48, 553-559 (2010).

[12]

Preedy, V. Tea in Health and Disease Prevention (Academic Press, 2013).

[13]

Yang, Z., Baldermann, S. & Watanabe, N. Recent studies of the volatile compounds in tea. Food Res. Int. 53, 585-599 (2013).

[14]

Daglia, M., Antiochia, R., Sobolev, A. P. & Mannina, L. Untargeted and targeted methodologies in the study of tea (Camellia sinensis L.). Food Res. Int. 63, 275-289 (2014).

[15]

Dudareva, N., Klempien, A., Muhlemann, J. K. & Kaplan, I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. N. Phytol. 198, 16-32 (2013).

[16]

Zeng, L., Watanabe, N. & Yang, Z. Understanding the biosyntheses and stress response mechanisms of aroma compounds in tea (Camellia sinensis) to safely and effectively improve tea aroma. Crit. Rev. Food Sci. 59, 2321-2334 (2019).

[17]

Xin, Z. et al. A putative 12-oxophytodienoate reductase gene CsOPR3 from Camellia sinensis, is involved in wound and herbivore infestation responses. Gene 615, 18-24 (2017).

[18]

Xu, Y. et al. Identification and expression profiling of the auxin response factors (ARFs) in the tea plant (Camellia sinensis (L.) O. Kuntze) under various abiotic stresses. Plant Physiol. Biochem. 98, 46-56 (2016).

[19]

Song, D., Jaganathan, G. K., Han, Y. & Liu, B. Seed dormancy in Camellia sinensis L.(Theaceae): effects of cold-stratification and exogenous gibberellic acid application on germination. Botany 95, 147-152 (2017).

[20]

Shang, Y. & Huang, S. Multi‐omics data‐driven investigations of metabolic diversity of plant triterpenoids. Plant J. 97, 101-111 (2019).

[21]

Zheng, C. et al. Integrated RNA-Seq and sRNA-Seq analysis identifies chilling and freezing responsive key molecular players and pathways in tea plant (Camellia sinensis). PLoS ONE 10, e0125031 (2015).

[22]

Ma, C. et al. Phenotypic, histological and proteomic analyses reveal multiple differences associated with chloroplast development in yellow and variegated variants from Camellia sinensis. Sci. Rep. 6, e33369 (2016).

[23]

Dai, W. et al. Characterization of white tea metabolome: comparison against green and black tea by a nontargeted metabolomics approach. Food Res. Int. 96, 40-45 (2017).

[24]

Rajasundaram, D. & Selbig, J. More effort-more results: recent advances in integrative ‘omics’ data analysis. Curr. Opin. Plant Biol. 30, 57-61 (2016).

[25]

Rai, A., Saito, K. & Yamazaki, M. Integrated omics analysis of specialized metabolism in medicinal plants. Plant J. 90, 764-787 (2017).

[26]

Shi, J. et al. Methyl jasmonate-induced changes of flavor profiles during the processing of green, oolong, and black tea. Front. Plant Sci. 14, e781 (2019).

[27]

Shi, J. et al. Transcriptional responses and flavor volatiles biosynthesis in methyl jasmonate-treated tea leaves. BMC Plant Biol. 15, e233 (2015).

[28]

Christensen, S. A. et al. The maize lipoxygenase, Zm LOX 10, mediates green leaf volatile, jasmonate and herbivore‐induced plant volatile production for defense against insect attack. Plant J. 74, 59-73 (2013).

[29]

Ul, H., Zainal, Z. & Ismail, I. Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology. Plant Biotechnol. J. 13, 727-739 (2015).

[30]

Seo, H. S. et al. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc. Natl Acad. Sci. USA 98, 4788-4793 (2001).

[31]

Fonseca, S. et al. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344-350 (2009).

[32]

Santino, A. et al. Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep. 32, 1085-1098 (2013).

[33]

Li, X., Schuler, M. A. & Berenbaum, M. R. Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419, 712-715 (2020).

[34]

Haroth, S. et al. The glycosyltransferase UGT76E1 significantly contributes to 12-O-glucopyranosyl-jasmonic acid formation in wounded Arabidopsis thaliana leaves. J. Biol. Chem. 294, 9858-9872 (2019).

[35]

Liang, Z. et al. Glycosidically bound aroma precursors in fruits: A comprehensive review. Crit. Rev. Food Sci. Nutr. 3, 1-29 (2020).

[36]

Banerjee, A. & Hamberger, B. P450s controlling metabolic bifurcations in plant terpene specialized metabolism. Phytochem. Rev. 17, 81-111 (2018).

[37]

Ho, C. T., Zheng, X. & Li, S. Tea aroma formation. Food Sci. Hum. Well. 4, 9-27 (2015).

[38]

Song, C., Härtl, K., McGraphery, K., Hoffmann, T. & Schwab, W. Attractive but toxic: emerging roles of glycosidically bound volatiles and glycosyltransferases involved in their formation. Mol. Plant 11, 1225-1236 (2018).

[39]

Ohnishi, T. Aroma Glycosides Contribute Plant Chemical Defense. Green. Sci. Technol. 16, e145 (2019).

[40]

Li, P. et al. Variation patterns in the content of glycosides during green tea manufacturing by a modification-specific metabolomics approach: Enzymatic reaction promoting an increase in the glycosidically bound volatiles at the pan firing stage. Food Chem. 279, 80-87 (2019).

[41]

Gui, J. et al. Does enzymatic hydrolysis of glycosidically bound volatile compounds really contribute to the formation of volatile compounds during the oolong tea manufacturing process? J. Agric. Food Chem. 63, 6905-6914 (2015).

[42]

Zeng, L. et al. Elucidation of (Z)-3-hexenyl-β-glucopyranoside enhancement mechanism under stresses from the oolong tea manufacturing process. J. Agric. Food Chem. 67, 6541-6550 (2019).

[43]

Feussner, I. The glycosyltransferase UGT76E1 significantly contributes to 12-O-glucopyranosyl-jasmonic acid formation in wounded Arabidopsis thaliana leaves. J. Biol. Chem. 294, 9858-9872 (2019).

[44]

Wei, C. et al. Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. P. Natl Acad. Sci. U. S. A 115, e4151-e4158 (2018).

[45]

Sato, K., Matsuo, T. & Mizutani, K. Characteristic fluctuations in glycosidically bound volatiles during tea processing and identification of their unstable derivatives. J. Agric. Food Chem. 64, 1151-1157 (2016).

[46]

Mageney, V., Baldermann, S. & Albach, D. C. Intraspecific variation in carotenoids of brassica oleracea var. sabellica. J. Agric. Food Chem. 64, 3251-3257 (2016).

PDF (2491KB)

5

Accesses

0

Citation

Detail

Sections
Recommended

/