Abstract
To improving the understand of the accumulation pattern of soluble sugars in Magnolia wufengensis during natural cold acclimation, the dynamics of freezing tolerance, the content of various soluble sugars in the shoots of M. wufengensis seedlings treated with salicylic acid, and the correlation between them were analyzed from September 2017 to March 2018. Salicylic acid advanced the natural cold acclimation and ultimately enhanced mid-winter hardiness by promoting the accumulation of total soluble sugars. Improved freezing tolerance highly correlated with enhanced glucose, fructose, and raffinose accumulation. The enhanced accumulation of these sugars by elevated amylase, sucrose synthase, and sucrose-P-synthase activities may contribute to advanced natural cold acclimation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Arora R, Wisniewski ME, Scorza R (1992) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiol 99:1562–1568. https://doi.org/10.1104/pp.99.4.1562
Bravo A, Zuniga GE, Alberdi M, Corcuera LJ (1998) The role of ABA in freezing tolerance and cold acclimation. Physiol Plantarum 103:17–23. https://doi.org/10.1034/j.1399-3054.1998.1030103.x
Cao YY, Yang MT, Li X, Zhou ZQ, Wang XJ, Bai JG (2014) Exogenous sucrose increases chilling tolerance in cucumber seedlings by modulating antioxidant enzyme activity and regulating proline and soluble sugar contents. Sci Horti 179:67–77. https://doi.org/10.1016/j.scienta.2014.09.016
Cardemil L, Varner JE (1984) Starch degradation metabolism towards sucrose synthesis in germinating Araucaria araucana seeds. Plant Physiol 76:1047–1054. https://doi.org/10.2307/4269054
Chan ZL, Wang Q, Xu XB, Meng XH, Qin GZ, Li BQ, Tian SP (2008) Functions of defense-related proteins and dehydrogenases in resistance response induced by salicylic acid in sweet cherry fruits at different maturity stages. Proteomics 8:4791–4807. https://doi.org/10.1002/pmic.200701155
Charrier G, Ameglio T (2011) The timing of leaf fall affects cold acclimation by interactions with air temperature through water and carbohydrate contents. Environ Exp Bot 72:351–357. https://doi.org/10.1016/j.envexpbot.2010.12.019
Doehlert DC, Duke SH, Anderson L (1982) Beta-amylases from alfalfa (Medicago sativa L.) roots. Plant Physiol 69:1096–1102. https://doi.org/10.1104/pp.69.5.1096
Dong CJ, Wang XL, Shang QM (2011) Salicylic acid regulates sugar metabolism that confers tolerance to salinity stress in cucumber seedlings. Sci Hortic. https://doi.org/10.1016/j.scienta.2011.05.005
Duan XJ, Cai CH, Yang Y, Chen FJ, Sang ZY, Ma LY (2019) Fall ethephon application enhances the freezing tolerance of Magnolia wufengensis during overwintering. Forests 10(10):868. https://doi.org/10.3390/f10100868
Flinn CL, Ashworth EN (1995) The relationship between carbohydrates and flower bud hardiness among three Forsythia taxa. J Am Soc Hortic Sci 120:607–613
Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Ryals KJ (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261(5122):754–756. https://doi.org/10.1126/science.261.5122.754.
Gusta LV, Wisniewski M, Nesbitt NT, Gusta ML (2004) The effect of water, sugars and proteins on the pattern of ice nucleation and propagation in acclimated an non-acclimated canola leaves. Plant Physiol 135:1642–1653. https://doi.org/10.2307/4356521
Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100:502–508. https://doi.org/10.2307/4274654
Imanishi HT, Suzuki T, Masuda K, Harada T (1988) Accumulation of raffinose and stachyose in shoot apices of Lonicera caerulea L. during cold acclimation. Sci Hortic 72:255–263. https://doi.org/10.1016/s0304-4238(97)00129-5
Janda T, Horváth E, Szalai C, Paldi E (2007) Role of salicylic acid in the induction of abiotic stress tolerance. In: Hayat S, Ahmad A (eds) Salicylic acid: a plant hormone. Springer, Dordrecht, pp 91–154
Jun HL, Duk JY, Su JK, Doil C, Hee JL (2012) Intraspecies differences in cold hardiness, carbohydrate content and β-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiol 32:1533–1540. https://doi.org/10.1093/treephys/tps102
Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plantarum 115:571–576. https://doi.org/10.1034/j.1399-3054.2002.1150411.x
Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperatures stress. Physiol Plantarum 126:120–128. https://doi.org/10.1111/j.1399-3054.2006.00604.x
Kasuga J, Arakawa K, Fujikawa S (2007) High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol 174:569–579. https://doi.org/10.1111/j.1469-8137.2007.02025.x
Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255. https://doi.org/10.1111/pce.12061
Krasensky J, Jonak C (2012) Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1–16. https://doi.org/10.1093/jxb/err460
Lee JH, Yu DJ, Kim SJ, Choi D, Lee HJ (2012) Intraspecies differences in cold hardiness, carbohydrate content and beta-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiol 32:1533–1540. https://doi.org/10.1093/treephys/tps102
Li HS (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing, pp 194–197
Lim CC, Arora R (1998) Comparing Gompertz and Richards functions to estimate freezing injury in Rhododendron using electrolyte leakage. J Am Soc Hortic Sci 123:246–252
Liu F, Jensen CR, Andersen MN (2004) Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crop Res 86:1–13. https://doi.org/10.1016/s0378-4290(03)00165-5
Ma LY, Wang LR, He SC, Liu X, Wang XQ (2006b) A new variety of Magnolia(Magnoliaceae) from Hubei, China. Bull Bot Res 26:517–519
Ma LY, Wang LR, He SC, Liu X, Wang XQ (2006a) A new species of Magnolia(Magnoliaceae) from Hubei, China. Bull Bot Res 26:4–7
Ma J, Deng SX, Jia ZK, Sang ZY, Zhu ZL, Zhou C, Ma LY, Chen FJ (2019) Conservation and divergence of ancestral AGAMOUS/SEEDSTICK subfamily genes from the basal angiosperm Magnolia wufengensis. Tree Physiol. https://doi.org/10.1093/treephys/tpz091
Morin X, Améglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, Miglietta F, Chuine I (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27:817–825. https://doi.org/10.1093/treephys/27.6.817
Mutlu S, Karadaolu O, Atici O, Nalbantolu B (2013) Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol Plantarum 57(3):507–513. https://doi.org/10.1007/s10535-013-0322-4
Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815. https://doi.org/10.1016/j.jplph.2010.11.001
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. https://doi.org/10.1104/pp.108.122465
Palonen P, Buszard D, Donnelly D (2000) Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Plantarum 110:393–401. https://doi.org/10.1111/j.1399-3054.2000.1100314.x
Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424. https://doi.org/10.1006/anbo.2000.1352
Pociecha E, Paek A, Janowiak F, Waligórski P, Zwierzykowski Z (2010) Changes in abscisic acid, salicylic acid and phenylpropanoid concentrations during cold acclimation of androgenic forms of festulolium (festuca pratensis × lolium multiflorum) in relation to resistance to pink snow mould (Microdochium nivale). Plant Breed 128(4):397–403. https://doi.org/10.1111/j.1439-0523.2009.01664.x
Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923. https://doi.org/10.1104/pp.106.082057
Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59:4205–4217. https://doi.org/10.1093/jxb/ern262
Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67. https://doi.org/10.1146/annurev-arplant-050213-040251
Sang ZY, Ma LY, Chen FJ, Zhang P, Zhu YC (2011) Protection status and utilization countermeasure of germplasm resources of the Magnolia wufengensis in Wufeng County. Hubei Agric Sci 50:1564–1567
Shao HB, Liang ZS, Shao MA (2006) Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloid Surf B 47:132–139. https://doi.org/10.1016/j.colsurfb.2005.11.028
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141. https://doi.org/10.1023/a:1022556103536
Suojala T, Lindén L (1997) Frost hardiness of Philadelphus and Hydrangea clones during ecodormancy. Acta Agr Scand 47:58–63
Tarchevsky IA, Yakovleva VG, Egorova AM (2010) Proteomic analysis of salicylate-induced proteins of pea (Pisum sativum L.) leaves. Biochemistry 75:590–597. https://doi.org/10.1134/S0006297910050081
Tasgín E, Atící Ö, Nalbantoglu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236. https://doi.org/10.1023/b:grow.0000007504.41476.c2
Teets TM, Hummel RL, Guy CL (1989) Cold-acclimation of Hibiscus rosasinensis L. and Hybiscus syriacus L. in natural and controlled environments. Plant Cell Environ 12:495–502. https://doi.org/10.1111/j.1365-3040.1989.tb02122.x
Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206. https://doi.org/10.1146/annurev.phyto.050908.135202
Wang LJ, Li SH (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694. https://doi.org/10.1016/j.plantsci.2005.09.005
Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:e123. https://doi.org/10.1371/journal.ppat.0020123
Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169:1269–1278. https://doi.org/10.1126/science.169.3952.1269
Yang Y, Jia ZK, Chen FJ, Sang ZY, Ma LY (2015c) Physiological and biochemical processes of Magnolia wufengensis in response to foliar abscisic acid application during natural cold acclimation. HortScience 50:387–394
Yang Y, Jia ZK, Chen FJ, Sang ZY, Duan J, Ma LY (2015b) Natural cold acclimatisation and de-acclimatisation of Magnolia wufengensis in response to alternative methods of application of abscisic acid. J Hortic Sci Biotech 90:704–710. https://doi.org/10.1080/14620316.2015.11668734
Yang Y, Jia ZK, Chen FJ, Sang ZY, Ma LY (2015a) Comparative analysis of natural cold acclimation and de-acclimation of two Magnolia species with different winter hardiness. Acta Physiol Plantarum 37:129. https://doi.org/10.1007/s11738-015-1883-y
Yang Y, Jia ZK, Chen FJ, Sang ZY, Duan J, Ma LY (2016) Effect of exogenous abscisic acid on cold acclimation in two Magnolia species. Biol Plantarum 60:555–562. https://doi.org/10.1007/s10535-016-0623-5
Yu J, Cang JC, Li Y, Huang R, Lu QW, Wang XT, Liu LJ, Xu QH, Zhang KJ (2016) Salicylic acid-induced antioxidant protection against low temperature in cold-hardy winter wheat. Acta Physiol Plant 38(11):261. https://doi.org/10.1007/s11738-016-2272-x
Yue C, Cao HL, Wang L, Zhou YH, Huang YT, Hao XY, Wang YC, Wang B, Yang YJ, Wang XC (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88(6):591–608. https://doi.org/10.1007/s11103-015-0345-7
Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. https://doi.org/10.1146/annurev-arplant-042809-112301
Acknowledgements
We are thankful to Wufeng Bo Ling Magnolia wufengensis Technology Development Co., Ltd. for providing Magnolia wufengensis seedlings. And, we gratefully acknowledge anonymous reviewers for their helpful comments on this manuscript.
Funding
This research was financially supported by the Special Fund for Forest Scientific Research in the Public Welfare (Grant No. 201504704).
Author information
Authors and Affiliations
Contributions
XD designing the experiments, doing the experiments, running data analyses and writing the paper; ZZ designing the experiments partly, running data analyses and supervising the work; YY designing the experiments and supervising the work; JD, ZJ and FC coordinating and supervising the work; ZS coordinating, supervising and partly financially supporting work; LM conceiving and designing the experiments, supervising the work; All the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Handling Editor: Tibor Janda.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Duan, X., Zhu, Z., Yang, Y. et al. Salicylic Acid Regulates Sugar Metabolism that Confers Freezing Tolerance in Magnolia wufengensis During Natural Cold Acclimation. J Plant Growth Regul 41, 227–235 (2022). https://doi.org/10.1007/s00344-020-10281-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-020-10281-3