The white water lily ( Nymphaea candida ), exemplifying nature’s resilience, thrives in the high-altitude terrains of Xinjiang, China, serving as an ideal model for investigating cold adaptation mechanisms in aquatic plants. This study meticulously elucidates the complex cold adaptation mechanisms of the white water lily through a comprehensive and integrated methodological approach. We discovered that the water lily undergoes ecodormancy in winter, retaining high cellular viability and growth potential. During overwintering, the white water lily demonstrates effective resource reallocation, a process facilitated by morphological adjustments, thereby strengthening its resistance to cold temperatures. This enhancement is achieved particularly through the compartmentalization of large vacuoles, the accumulation of osmoregulatory substances, and an increased antioxidant capacity. We established the first exhaustive full-length transcriptome for the white water lily. A subsequent comprehensive analysis of the transcriptome, phytohormones, and metabolome uncovered a multifaceted regulatory network orchestrating cold adaptation. Our research spotlights phytohormone signaling, amino acid metabolism, and circadian rhythms as key elements in the water lily’s defense against cold. The results emphasize the critical role of nitrogen metabolism, especially amino acid-related pathways, during cold stress. Metabolite profiling revealed the importance of compounds like myo-inositol and L-proline in enhancing cold tolerance. Remarkably, our study demonstrates that the white water lily notably diminishes the utilization of unsaturated fatty acids in its temperature regulation strategies. In conclusion, this research substantially enriches our understanding of the white water lily’s intricate cold adaptation mechanisms, offering new perspectives on the adaptive strategies of aquatic plants and potential applications in agricultural advancement.
Acknowledgements
This research was funded by the National Natural Science Foundation of China (no. U2003113; U1803104; 31971710); China Postdoctoral Science Foundation (2505BSHJJ); A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.
Data availability statement
The raw sequencing data that support the findings of this study have been deposited into CNGB Sequence Archive (CNSA) of China National GeneBank DataBase (CNGBdb) with project accession number CNP0005037.
Conflict of interests
The authors declare no conflict of interest.
Supplementary information
Supplementary data is available at Horticulture Research online.
| [1] |
Bai H, Liao X, Li X. et al. DgbZIP3 interacts with DgbZIP2 to increase the expression of DgPOD for cold stress tolerance in chrysanthemum. Hortic Res. 2022; 9 :uhac105
|
| [2] |
Theocharis A, Clément C, Barka EA. Physiological and molecular changes in plants grown at low temperatures. Planta. 2012; 235 : 1091-105
|
| [3] |
Raza A, Charagh S, Abbas S. et al. Assessment of proline function in higher plants under extreme temperatures. Plant Biol. 2023; 25 : 379-95
|
| [4] |
Zhao L, Yang T, Xing C. et al. The β-amylase PbrBAM3 from pear ( Pyrus betulaefolia ) regulates soluble sugar accumulation and ROS homeostasis in response to cold stress. Plant Sci. 2019; 287 :110184
|
| [5] |
Zhao Y, Liu C, Sui J. et al. A wake-up call: signaling in regulating ornamental geophytes dormancy. Orn Plant Res. 2022; 2 :8
|
| [6] |
Zhou W, Chen F, Luo X. et al. A matter of life and death: molecular, physiological, and environmental regulation of seed longevity. Plant Cell Environ. 2020; 43 :293-302
|
| [7] |
Bhattacharya A. Lipid metabolism in plants under low-temperature stress:a review. In: Bhattacharya A,ed. Physiological Processes in Plants Under Low Temperature Stress. Singapore: Springer, 2022, 409-516
|
| [8] |
Liu B, Zhao F-M, Cao Y. et al. Photoprotection contributes to freezing tolerance as revealed by RNA-seq profiling of rhododendron leaves during cold acclimation and deacclimation over time. Hortic Res. 2022; 9 :uhab025
|
| [9] |
Li M, Duan X, Gao G. et al. CmABF1 and CmCBF4 cooperatively regulate putrescine synthesis to improve cold tolerance of melon seedlings. Hortic Res. 2022; 9 :uhac002
|
| [10] |
Liu Y, Dang P, Liu L. et al. Cold acclimation by the CBF-COR pathway in a changing climate: lessons from Arabidopsis thaliana. Plant Cell Rep. 2019; 38 :511-9
|
| [11] |
Zhang L, Jiang X, Liu Q. et al. The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ. 2020; 43 :2712-26
|
| [12] |
Chen F, Liu X, Yu C. et al. Water lilies as emerging models for Darwin’s abominable mystery. Hortic Res. 2017; 4 :17051
|
| [13] |
Xiong X, Zhang J, Yang Y. et al. Water lily research: past, present, and future. Tropical Plants. 2023; 2 :1-8
|
| [14] |
Zhang L, Chen F, Zhang X. et al. The water lily genome and the early evolution of flowering plants. Nat Plants. 2020; 577 :79-84
|
| [15] |
Povilus RA, DaCosta JM, Grassa C. et al. Water lily ( Nymphaea ther- marum ) genome reveals variable genomic signatures of ancient vascular cambium losses. Proc Natl Acad Sci. 2020; 117 :8649-56
|
| [16] |
Yang Y, Sun P, Lv L. et al. Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution. Nat Plants. 2020; 6 :215-22
|
| [17] |
Yu C, Qiao G, Qiu W. et al. Molecular breeding of water lily: engineering cold stress tolerance into tropical water lily. Hortic Res. 2018; 5 :73
|
| [18] |
Khan WU, Khan LU, Chen D. et al. Comparative analyses of superoxide dismutase (SOD) gene family and expression profiling under multiple abiotic stresses in water lilies. Horticulturae. 2023; 9 :781
|
| [19] |
Ma X, Jin Q, Wang Y. et al. Comparative transcriptome analysis reveals the regulatory mechanisms of two tropical water lilies in response to cold stress. BMC Genomics. 2023; 24 :1-21
|
| [20] |
Ashraf MA, Rahman A. Hormonal regulation of cold stress response. In: Wani SH, Herath V (eds.), Cold Tolerance in Plants: Physiological, Molecular and Genetic Perspectives. Cham: Springer, 2018, 65-88
|
| [21] |
Aghdam MS, Moradi M, Razavi F. et al. Exogenous phenylalanine application promotes chilling tolerance in tomato fruits during cold storage by ensuring supply of NADPH for activation of ROS scavenging systems. Sci Hortic. 2019; 246 :818-25
|
| [22] |
Han M, Xu M, Wang S. et al. Effects of exogenous L-glutamine as a sole nitrogen source on physiological characteristics and nitrogen use efficiency of poplar. Plant Physiol Biochem. 2022; 172 : 1-13
|
| [23] |
Jozefczak M, Keunen E, Schat H. et al. Differential response of Arabidopsis leaves and roots to cadmium: glutathione-related chelating capacity vs antioxidant capacity. Plant Physiol Biochem. 2014; 83 :1-9
|
| [24] |
Zhang M, Viennois E, Prasad M. et al. Edible ginger-derived nanoparticles: a novel therapeutic approach for the prevention and treatment of inflammatory bowel disease and colitis-associated cancer. Biomaterials. 2016; 101 :321-40
|
| [25] |
Lee SH, Singh AP, Chung GC. et al. Chilling root temperature causes rapid ultrastructural changes in cortical cells of cucumber (Cucumis sativus L.) root tips. J Exp Bot. 2002; 53 : 2225-37
|
| [26] |
Li S-L, Li Z-G, Yang L-T. et al. Differential effects of cold stress on chloroplasts structures and photosynthetic characteristics in cold-sensitive and cold-tolerant cultivars of sugarcane. Sugar Tech. 2018; 20 :11-20
|
| [27] |
Pagliarani C, Moine A, Chitarra W. et al. The C4 protein of tomato yellow leaf curl Sardinia virus primes drought tolerance in tomato through morphological adjustments. Hortic Res. 2022; 9 :uhac164
|
| [28] |
Guy C, Kaplan F, Kopka J. et al. Metabolomics of temperature stress. Physiol Plant. 2008; 132 :220-35
|
| [29] |
Gillaspy GE. The role of phosphoinositides and inositol phosphates in plant cell signaling. In: Capelluto DGS,ed. Lipid-mediated Protein Signaling. Dordrecht: Springer, 2013, 141-57
|
| [30] |
Hermann J, Noels H, Theelen W. et al. Sample preparation of formalin-fixed paraffin-embedded tissue sections for MALDI-mass spectrometry imaging. Anal Bioanal Chem. 2020; 412 : 1263-75
|
| [31] |
Wolberg S, Haim M, Shtein I. Simple differential staining method of paraffin-embedded plant sections with safranin-alcian blue. IAWA J. 2023; 44 :170-5
|
| [32] |
Ozturk OK, Kaasgaard SG, Palmén LG. et al. Enzyme treatments on corn fiber from wet-milling process for increased starch and protein extraction. Ind Crop Prod. 2021; 168 :113622
|
| [33] |
Huang C, Kurotani KI, Tabata R. et al. Nicotiana benthamiana XYLEM CYSTEINE PROTEASE genes facilitate tracheary element formation in interfamily grafting. Hortic Res. 2023; 10 :uhad072
|
| [34] |
Zhang L, Wang C, Jia R. et al. Malate metabolism mediated by the cytoplasmic malate dehydrogenase gene MdcyMDH affects sucrose synthesis in apple fruit. Hortic Res. 2022; 9 :uhac194
|
| [35] |
Zhuang K, Kong F, Zhang S. et al. Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. New Phytol. 2019; 221 : 1998-2012
|
| [36] |
Jin Q, Zhu K, Cui W. et al. Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ. 2013; 36 :956-69
|
| [37] |
Li W, Meng R, Liu Y. et al. Heterografted chrysanthemums enhance salt stress tolerance by integrating reactive oxygen species, soluble sugar, and proline. Hortic Res. 2022; 9 :uhac073
|
| [38] |
Barretto SS, Michoux F, Hellgardt K. et al. Pneumatic hydrodynamics influence transplastomic protein yields and biological responses during in vitro shoot regeneration of Nicotiana tabacum callus: implications for bioprocess routes to plant-made pharmaceuticals. Biochem Eng J. 2017; 117 :73-81
|
| [39] |
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12 :1-16
|
| [40] |
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15 :1-21
|
| [41] |
Szklarczyk D, Franceschini A, Wyder S. et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015; 43 :D447-52
|
| [42] |
Hwarari D, Guan Y, Ahmad B. et al. ICECBF-COR signaling cascade and its regulation in plants responding to cold stress. Int J Mol Sci. 2022; 23 :1549
|
| [43] |
Fornara F, de Montaigu A, Sánchez-Villarreal A. et al. The GI-CDF module of Arabidopsis affects freezing tolerance and growth as well as flowering. Plant J. 2015; 81 :695-706
|
| [44] |
Hasanuzzaman M, Bhuyan MB, Zulfiqar F. et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants. 2020; 9 :681
|
| [45] |
Yang Y-B, Yin J, Huang L-Q. et al. Salt enhances disease resistance and suppresses cell death in ceramide kinase mutants. Plant Physiol. 2019; 181 :319-31
|
| [46] |
Nawaz M, Hassan MU, Chattha MU. et al. Trehalose: A promising osmo-protectant against salinity stress-physiological and molecular mechanisms and future prospective. Mol Biol Rep. 2022; 49 :11255-71
|
| [47] |
Jin H, Sun Y, Yang Q. et al. Screening of genes induced by salt stress from Alfalfa. Mol Biol Rep. 2010; 37 :745-53
|