Abstract
Successful winter survival of the plants needs a programmed capacity to activate appropriate mechanisms in development of frost tolerance (FT). Cold hardening is a complicated operation facilitating the overwintering and is associated by extensive changes in metabolome. The purpose of the present investigation is to simplify the association between metabolites changes and FT in winter rye varieties (Puma and Anatolien) acclimated under field situation in NW Iran, regions with long winters. Plants were sampled on five dates (Oct. 31, Nov. 29, Dec. 17, Jan. 4, and Feb. 1) as different cold hardening periods. FT, as measured by LT50 (the temperature at 50% lethality) significantly expanded during the autumn and winter seasons. Cold adaptation persuaded accumulation of sucrose and sorbitol in both varieties; however, the accumulation was more profound in Puma. The content of proline, aspartic acid, glutamic acid, tyrosine, and glycine betaine linearly expanded in the Anatolien variety during the overwintering. However, content of glycine betaine, proline, and aspartic acid in Puma was considerably higher than Anatolien. Hydrogen peroxide reached to its greatest quantities at November and December in Anatolien and Puma, respectively. These levels significantly reduced up to the next months. Glutathione and ascorbic acid contents, as important antioxidants, noticeably expanded during overwintering. There was a significant positive association between FT, total protein content, free amino acid, soluble sugars, and glycine betaine. These data suggest that the development of FT during the cold adaptation and overwintering is partly resulted from metabolome changes and such modifications are strongly linked to the genetic potential.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aretz I, Meierhofer D (2016) Advantages and pitfalls of mass spectrometry based metabolome profiling in systems biology. Int J Mol Sci 17(5):632. https://doi.org/10.3390/ijms17050632
Artlip TS, Callahan AM, Bassett CL, Wisniewski ME (1997) Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica [L.] Batsch). Plant Mol Biol 33(1):61–70. https://doi.org/10.1023/A:1005787909506
Benson EE (2008) Cryopreservation theory. Plant cryopreservation: a practical guide. Springer, Berlin, pp 15–32. https://doi.org/10.1007/978-0-387-72276-4_1
Bhandari K, Nayyar H (2014) Low temperature stress in plants: an overview of roles of cryoprotectants in defense. In: Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 193–265. https://doi.org/10.1007/978-1-4614-8591-9_9
Caverzan A, Casassola A, Brammer SP (2016) Antioxidant responses of wheat plants under stress. Genet Mol Biol 39(1):1–6. https://doi.org/10.1590/1678-4685-GMB-2015-0109
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17(8):1043–1054. https://doi.org/10.1101/gad.1077503
Dai F, Huang Y, Zhou M, Zhang G (2009) The influence of cold acclimation on antioxidative enzymes and antioxidants in sensitive and tolerant barley cultivars. Biol Plant 53(2):257–262. https://doi.org/10.1007/s10535-009-0048-5
Dionne J, Castonguay Y, Nadeau P, Desjardins Y (2001) Amino acid and protein changes during cold acclimation of green-type annual bluegrass ecotypes. Crop Sci 41(6):1862–1870. https://doi.org/10.2135/cropsci2001.1862
Ershadi A, Karimi R, Mahdei KN (2016) Freezing tolerance and its relationship with soluble carbohydrates, proline and water content in 12 grapevine cultivars. Acta Physiol Plant 38(1):2–10. https://doi.org/10.1007/s11738-015-2021-6
Fowler DB (2008) Cold acclimation threshold induction temperatures in cereals. Crop Sci 48(3):1147–1154. https://doi.org/10.2135/cropsci2007.10.0581
Gol L, Tomé F, von Korff M (2017) Floral transitions in wheat and barley: interactions between photoperiod, abiotic stresses, and nutrient status. J Exp Bot 68(7):1399–1410. https://doi.org/10.1093/jxb/erx055
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70(2):303–307. https://doi.org/10.1007/bf02374789
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212. https://doi.org/10.1016/0003-2697(80)90139-6
Gulyás Z, Boldizsár Á, Novák A, Szalai G, Pál M, Galiba G, Kocsy G (2014) Central role of the flowering repressor ZCCT2 in the redox control of freezing tolerance and the initial development of flower primordia in wheat. BMC Plant Biol 14(1):91. https://doi.org/10.1186/1471-2229-14-91
Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of abscisic acid. J Plant Growth Regul 24(4):308–318. https://doi.org/10.1007/s00344-005-0079-x
Hameed A, Gulzar S, Aziz I, Hussain T, Gul B, Khan MA (2015) Effects of salinity and ascorbic acid on growth, water status and antioxidant system in a perennial halophyte. AoBPlants 7:plv004. https://doi.org/10.1093/aobpla/plv004
Hayat S, Hayat Q, Alyemen MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466. https://doi.org/10.4161/psb.21949
Herman EM, Rotter K, Premakumar R, Elwinger G, Bae R, Ehler-King L, Chen S, Livingston DP III (2006) Additional freeze hardiness in wheat acquired by exposure to − 3 °C is associated with extensive physiological, morphological, and molecular changes. J Exp Bot 57(14):3601–3618. https://doi.org/10.1093/jxb/erl111
Hosseini M, Maali-Amiri R, Mahfoozi S, Fowler DB, Mohammadi R (2016) Developmental regulation of metabolites and low temperature tolerance in lines of crosses between spring and winter wheat. Acta Physiol Plant 38(4):87. https://doi.org/10.1007/s11738-016-2103-0
Janmohammadi M (2012) Cold acclimation and vegetative/reproductive transition in winter cereals. Albanian J Agric Sci 11(4):199–205. https://sites.google.com/a/ubt.edu.al/rssb/
Janmohammadi M, Enayati V, Sabaghnia N (2012a). Impact of cold acclimation, de-acclimation and re-acclimation on carbohydrate content and antioxidant enzyme activities in spring and winter wheat. Icel Agric Sci 25:3–11. http://hdl.handle.net/1946/19761
Janmohammadi M, Mahfoozi S, Tvakkol-Afshari R (2012b) Influence of vegetative/reproductive transition on proline and protein accumulation and expression of freezing tolerance in wheat cultivars grown in temperate and cold climates. Agric For 58(3):67–84. http://89.188.43.75/agricultforest/20130328-06
Janmohammadi M, Mock HP, Matros A (2014) Proteomic analysis of cold acclimation in winter wheat under field conditions. Icel Agric Sci 27:3–15
Kosová K, Prášil IT (2012) Annual field crops. Temperature adaptation in a changing climate: nature at risk. CABI, Oxfordshire, pp 186–207. https://doi.org/10.1079/9781845938222.0000
Koster KL, Lynch DV (1992) Solute accumulation and compartmentation during the cold acclimation of Puma rye. Plant Physiol 98(1):108–113. https://doi.org/10.1104/pp.98.1.108
Kozlowski TT, Pallardy SG (2002) Adaptation and adaptive responses of woody plants to environmental stresses. Bot Rev 68(2):270–334. https://doi.org/10.1663/0006-8101(2002)068%5B0270:AAAROW%5D2.0.CO;2
Landry EJ, Wolyn DJ (2012) A method to assess cold acclimation and freezing tolerance in asparagus seedlings. Can J Plant Sci 92(2):271–277. https://doi.org/10.4141/cjps2011-158
Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011. https://doi.org/10.1089/ars.2012.5074
Limin AE, Fowler DB (1988) Cold hardiness expression in interspecific hybrids and amphiploids of the Triticeae. Genome 30(3):361–365. https://doi.org/10.1139/g88-063
Livingston DP, Van K, Premakumar R, Tallury SP, Herman EM (2007) Using Arabidopsis thaliana as a model to study subzero acclimation in small grains. Cryobiology 54(2):154–163. https://doi.org/10.1016/j.cryobiol.2006.12.004
Mahfoozi S, Limin AE, Ahakpaz F, Fowler DB (2006) Phenological development and expression of freezing resistance in spring and winter wheat under field conditions in north-west Iran. Field Crops Res 97(2):182–187. https://doi.org/10.1016/j.fcr.2005.09.012
Morin X, Ameglio 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
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5(5):388–395. https://doi.org/10.1016/S1369-5266(02)00282-0
Okumoto S, Funck D, Trovato M, Forlani G (2016) Amino acids of the glutamate family: functions beyond primary metabolism. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00318
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 4(2):439–473. https://doi.org/10.1029/2006gl028098
Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45(4):481–487. https://doi.org/10.1023/A:1022308229759
Sabaghnia N, Ahadnezhad A, Janmohammdi M (2015) Genetic variation in garden cress (Lepidium sativum L.) germplasm as assessed by some morphological traits. Genet Resour Crop Evol 5(62):733–745. https://doi.org/10.1007/s10722-014-0192-4
Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer, Berlin. http://dx.doi.org/10.1007/978-3-642-71745-1
Schlegel RH (2013) Rye: genetics, breeding, and cultivation. CRC Press, Florida. https://doi.org/10.1201/b15553
Shahani S, Gohari AR, Monsef-Esfahani HR (2015) Quantification of sucrose in the root of Geum iranicum Khatamsaz. Pharm Biomed Sci Res 1(3):31–36. https://doi.org/10.18869/acadpub.pbr.1.3.31
Smallwood M, Bowle DJ (2002) Plants in a cold climate. Philos Trans R Soc Lond B Biol Sci 357(1423):831–847. https://doi.org/10.1098/rstb.2002.1073
Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiol Mol Biol Plants 14(1–2):69–79. https://doi.org/10.1007/s12298-008-0006-2
Thakur P, Nayyar H (2013) Facing the cold stress by plants in the changing environment: sensing, signaling, and defending mechanisms. In: Plant acclimation to environmental stress. Springer, New York, pp 29–69. https://doi.org/10.1007/978-1-4614-5001-6_2
Thomashow MF (1999) Plant cold adaptation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Phys Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Trischuk RG, Schilling BS, Low NH, Gray GR, Gusta LV (2014) Cold acclimation, de-acclimation and re-acclimation of spring canola, winter canola and winter wheat: the role of carbohydrates, cold-induced stress proteins and vernalization. Environ Exp Bot 106:156–163. https://doi.org/10.1016/j.envexpbot.2014.02.013
Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23(9):893–902. https://doi.org/10.1046/j.1365-3040.2000.00611.x
Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ (2012) Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem 60:141–149. https://doi.org/10.1016/j.plaphy.2012.07.010
Acknowledgements
This experiment was financially supported by a grant from university of Maragheh. In addition, the authors would like to thank experts of Central Laboratory (depended on Laboratory Network of Strategic Technologies) for their assistance in metabolome analysis.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Gao.
Rights and permissions
About this article
Cite this article
Janmohammadi, M., Sabaghnia, N. & Mahfoozi, S. Frost tolerance and metabolite changes of rye (Secale cereale) during the cold hardening and overwintering. Acta Physiol Plant 40, 42 (2018). https://doi.org/10.1007/s11738-018-2620-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-018-2620-0