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Unique Metabolic Shift Reveals Potential Mechanism of Cold and Freezing Acclimatization

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Abstract

Cold stress dramatically constrains crop yield and limits the geographical distribution of plants. However, the mechanism underlying cold and freezing acclimation in high-altitude medicinal plants, particularly, Picrorhiza kurroa remains unknown. Here, we have used three different temperature treatments, namely 4 °C 24 h, 4 °C 7D, and − 4 °C 24 h, to induce early cold stress, one-week cold stress, and freezing stress, respectively, in P. kurroa and utilized a metabolomic approach to decipher cold stress mitigation strategy. Temperature treatment caused wilting and necrosis of leaves, decreased photochemical reflective index, increased normalized plant chlorophyll index, anthocyanin reflectance index, and flavonol reflectance index. These biochemical changes are associated with the significant expression (p < 0.05) of 171 metabolites. The multivariate analysis leads to the identification of 31 (VIP > 1) from 171 metabolites contributing significant variance between control and cold/freezing stressed tissue. Differential metabolite expression leads to the alteration of 16 metabolic pathways with an impact of more than 0.1. The key metabolic pathways participating in induced cold/freezing acclimation are biosynthesis of secondary metabolites, flavone and flavonol biosynthesis, starch and sucrose metabolism, pyrimidine metabolism, butanoate metabolism, and fatty acid degradation, among others. The present analysis also showed that picroside is expressed differentially under cold/freezing stress, suggesting its role in cold/freezing acclimation. Further, this study provides a platform for future research in disentangling the role of identified metabolites and metabolic pathways putatively involved in cold/freezing stress response. In addition, identified metabolites could provide a basis for elucidating the evolution of metabolic response to cold/freezing stress.

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All the data presented in this manuscript are available in the supporting file of this manuscript.

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Acknowledgements

We acknowledge Director, CSIR-IHBT for providing research infrastructure. Satyakam is thankful to UGC for providing research fellowship. The manuscript has CSIR-IHBT publication number: 5254.

Funding

We thankful to DST-SERB (Grant, ECR/2017/000771/LS) and CSIR (Grant, MLP-201) for providing funds to support this research.

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RK conceived and designed the research work. Satyakam conducted the experiments. RK, RJ and Satyakam analyzed the data. RK and Satyakam wrote the manuscript. All authors edited and approved the manuscript.

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Correspondence to Rajiv Kumar.

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344_2023_10961_MOESM2_ESM.xls

Table S1 List of differentially abundant metabolites with intensity value and log2 values from P. kurroa under control, early cold stress (4 °C 24h), one-week cold stress (4 °C 7D), and freezing stress (-4 °C 24h) using UHPLC-MS.Supplementary file2 (XLS 205 KB)

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Satyakam, Joshi, R. & Kumar, R. Unique Metabolic Shift Reveals Potential Mechanism of Cold and Freezing Acclimatization. J Plant Growth Regul 42, 5763–5779 (2023). https://doi.org/10.1007/s00344-023-10961-w

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