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How Do Different Temperature Fluctuations Affect Alcea rosea ‘nigra’ Survival?

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Abstract

The warm gaps during cold weather will increase the risk of freezing damage to plants. The successful winter survival of hollyhock (Alcea rosea 'nigra') can be limited by climate warming. This study exposed the cold-acclimated and non-acclimated plants to warm and cold temperatures and determined their physiological and biochemical traits. The results showed that after acclimation, cold temperature effectively delayed the chilling injury, reduced the electrolyte leakage, significantly increased the activity of SOD, APX, and CAT, inhibited the content of hydrogen peroxide (H2O2), and retarded the increase in malondialdehyde (MDA) content, whereas they were increased in the other treatments. When non-cold and cold-acclimated plants were exposed to warm temperatures, a rapid decrease in antioxidant activities and osmolyte regulators occurred, resulting in a plant that no longer possesses an elevated level of freezing tolerance. Cold temperatures in non-acclimated plants did not induce substantial acclimation and reduced frost resistance primarily by limiting the water-soluble sugars and proline availability. The freezing tolerance of acclimated plants maintained a lower LT50 and exhibited higher net photosynthesis and stomatal conductance under freezing temperatures. Freezing tolerance in hollyhock plants (–6 °C) induced by suboptimal temperature acclimation is associated with enhanced photosynthetic adaptability, osmoregulation ability, and antioxidant activities.

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References

  • Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response to drought stress in ten cultivars of oil seed rape (Brassica napus L.). Czech J Genet PlantBreed 46:27–34

    Article  Google Scholar 

  • Ahmed I, Roy BC, Subramaniam D, Ganie SA, Kwatra D, Dixon D, Anant S, Afzal Zargar M, Umar S (2016) An ornamental plant targets epigenetic signaling to block cancer stem cell-driven colon carcinogenesis. Carcinogenesis 37:385–396. https://doi.org/10.1093/carcin/bgw009

    Article  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  Google Scholar 

  • Arfan M, Zhang DW, Zou LJ, Luo SS, Tan WR, Zhu T, Lin HH (2019) Hydrogen peroxide and nitric oxide crosstalk mediates brassinosteroids induced cold stress tolerance in Medicago truncatula. Int J Mol Sci 20:144. https://doi.org/10.3390/ijms20010144

    Article  Google Scholar 

  • Arias NS, Bucci SJ, Scholz FG, Goldstein G (2015) Freezing avoidance by supercooling in Olea europaea cultivars: the role of apoplastic water, solute content and cell wall rigidity. Plant Cell Environ 38:2061–2070. https://doi.org/10.1111/pce.12529

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolation chloroplast phenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  Google Scholar 

  • Baniulis D, Sirgėdienė M, Haimi P, Tamošiūnė I, Danusevičius D (2020) Constitutive and cold acclimation-regulated protein expression profiles of scots pine seedlings reveal potential for adaptive capacity of geographically distant populations. For 11:89. https://doi.org/10.3390/f11010089

    Article  Google Scholar 

  • Bao GZ, Tang WY, Zhou SJ, Liu BJ, Wu ZZ, Jin DX, Bian WJ, Zhu SN (2020) Photosynthesis characteristics of tall fescue under snow-melting agent, acid precipitation and freeze-thaw stress. Russ J Plant Physiol 67:529–537

    Article  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  Google Scholar 

  • Beheshti Rooy SS, Hosseini Salekdeh G, Ghabooli M, Gholami M, Karimi R (2017) Cold-induced physiological and biochemical responses of three grapevine cultivars differing in cold tolerance. Acta Physiol Plant 39:264. https://doi.org/10.1007/s11738-017-2561-z

    Article  Google Scholar 

  • Bertrand A, Rocher S, Claessens A, Bipfubusa M, Papadopoulos Y, Castonguay Y (2019) Biochemical and molecular responses during overwintering of red clover populations recurrently selected for improved freezing tolerance. Plant Sci. https://doi.org/10.1016/j.plantsci.2019.110388

    Article  Google Scholar 

  • Burbulis N, Jonytiene V, Kupreine R, Blinstrubiene A (2011a) Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro. J Food Agric Environ 99:371–374

    Google Scholar 

  • Burbulis N, Jonytienė V, Kuprienė R, Blinstrubienė A (2011b) Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro. J Food Agric Environ 9:371–374

    Google Scholar 

  • Campany CE, Medlyn BE, Duursma RA (2017) Reduced growth due to belowground sink limitation is not fully explained by reduced photosynthesis. Tree Physiol 37:1042–1054. https://doi.org/10.1093/treephys/tpx038

    Article  Google Scholar 

  • Chang CY, Bräutigam K, Hüner NPA, Ensminger I (2020) Champions of winter survival: Cold acclimation and molecular regulation of cold hardiness in evergreen conifers. New Phytol 229:675–691. https://doi.org/10.1111/nph.16904

    Article  Google Scholar 

  • Charier G, Lacointe A, Ameglio T (2018) Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut Trees Juglans regia L. Front Plant Sci 9:1746

    Article  Google Scholar 

  • Chen HH, Li PH (1980) Characteristics of cold acclimation and deacclimation in tuber-bearing solanum species. Plant Physiol 65:1146–1148. https://doi.org/10.1104/pp.65.6.1146

    Article  Google Scholar 

  • Cheong BE, Ho WWH, Biddulph B, Wallace X, Rathjen T, Rupasinghe TWT, Roessner U, Dolferus R (2019) Phenotyping reproductive stage chilling and frost tolerance in wheat using targeted metabolome and lipidome profiling. Metabolomics 15:144. https://doi.org/10.1007/s11306-019-1606-2

    Article  Google Scholar 

  • Cvetkovic J, Müller K, Baier M (2017) The effect of cold priming on the fitness of Arabidopsis thaliana accessions under natural and controlled conditions. Sci Rep 7:44055. https://doi.org/10.1038/srep44055

    Article  Google Scholar 

  • DaCosta M, Huang B (2007) Change in antioxidant activities and lipid peroxidation for bent-grass species in responses to drought stress. J Am Soc Hortic Sci 132:319–326

    Article  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Biochem 28:350–356

    Google Scholar 

  • Elkelish A, Qari SH, Mazrou YSA, Abdelaal KAA, Hafez YM, Abu-Elsaoud AM, Batiha GES, El-Esawi MA, El Nahhas N (2020) Exogenous ascorbic acid induced chilling tolerance in tomato plants through modulating metabolism, osmolytes, antioxidants, and transcriptional regulation of catalase and heat shock proteins. Plants 9:431

    Article  Google Scholar 

  • Fahmirad M, Karimzadeh G, Ghanati F (2013) Cold-induced changes of antioxidant enzymes activity and lipid peroxidation in two canola (Brassica napus L.) cultivars. J Plant Physiol Breed 3:1–11

    Google Scholar 

  • Fennell AY, Hoover E (1991) Photoperiod influences growth, bud dormancy, and cold acclimation in Vitis labruscana and V. Rparia Am Soc Hortic Sci 116:270–273. https://doi.org/10.21273/JASHS.116.2.270

    Article  Google Scholar 

  • Fürtauer L, Weiszmann J, Weckwerth W, Nägele T (2019) Dynamics of plant metabolism during cold acclimation. Inter J Mol Sci 20:5411. https://doi.org/10.3390/ijms20215411

    Article  Google Scholar 

  • Garcia-Molina A, Kleine T, Schneider K, Mühlhaus T, Lehmann M, Leister D (2020) Translational components contribute to acclimation responses to high light, heat, and cold in arabidopsis. Science 23:101331. https://doi.org/10.1016/j.isci.2020.101331

    Article  Google Scholar 

  • Gavelienė V, Pakalniškytė L, Novickienė L (2014) Regulation of proline and ethylene levels in rape seedlings for freezing tolerance. Open Life Sci 9:1099–1107. https://doi.org/10.2478/s11535-014-0340-z

    Article  Google Scholar 

  • Ghahreman A, Pakravan M, Assadi M (2000) A new species of Alcea (Malvaceae) from Iran. Nord J Bot 20:701–704. https://doi.org/10.1111/j.1756-1051.2000.tb00756.x

    Article  Google Scholar 

  • Guan X (2014) Physiology of cold acclimation and deacclimation responses of cool-season grasses: Carbon and hormone metabolism. Thesis. Master of Science (M.S. ).doi: https://doi.org/10.7275/6042177

  • Gusta LV, Wisniewski M, Nesbitt NT, Tanino KT (2003) Factors to consider in artificial freeze tests. Acta Hortic 618:493–507

    Article  Google Scholar 

  • Hajihashemi S, Noedoost F, Geuns JMC, Djalovic I, Siddique KHM (2018) Effect of cold stress on photosynthetic traits, carbohydrates, morphology, and anatomy in nine cultivars of Stevia rebaudiana. Front Plant Sci 9:1430. https://doi.org/10.3389/fpls.2018.01430

    Article  Google Scholar 

  • Han QH, Huang B, Ding CB, Zhang ZW, Chen YE, Hu C, Zhou LJ, Huang Y, Liao JQ, Yuan S, Yuan M (2017) Effects of melatonin on anti-oxidative systems and photosystem II in cold-stressed rice seedlings. Front Plant Sci 8:785. https://doi.org/10.3389/fpls.2017.00785

    Article  Google Scholar 

  • Hanna M, Janne K, Perttu V, Helena K (2018) Gaps in the capacity of modern forage crops to adapt to the changing climate in northern Europe. Mitig Adapt Strateg Glob Change 23:81–100. https://doi.org/10.1007/s11027-016-9729-5

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  Google Scholar 

  • Heil K, Lehner A, Schmidhalter U (2020) Influence of climate conditions on the temporal development of wheat yields in a long-term experiment in an area with pleistocene loess. Climate 8:100. https://doi.org/10.3390/cli8090100

    Article  Google Scholar 

  • Hussain L, Akash M, Tahir M, Rehman K, Ahmed K (2014) Hepatoprotective effects of methanolic extract of Alcea rosea against acetaminophen-induced hepatotoxicity in mice. Bangladesh J Pharmacol 9:322–327

    Google Scholar 

  • Hykkerud Steindal AL, Rødven R, Hansen E, Mølmann J (2015) Effects of photoperiod, growth temperature and cold acclimatisation on glucosinolates, sugars and fatty acids in kale. Food Chem 1:44–51. https://doi.org/10.1016/j.foodchem.2014.10.129

    Article  Google Scholar 

  • Jonytienė V, Burbulis N, Kuprienė R, Blinstrubienė A (2012) Effect of exogenous proline and de-acclimation treatment on cold tolerance in Brassica napus shoots cultured in vitro. J Food Agric Environ 10:327–330

    Google Scholar 

  • Kim J, Wolyn DJ (2014) Freezing tolerance assessment for seedlings of three asparagus cultivars grown under controlled conditions. Can J Plant Sci 95:495–504. https://doi.org/10.1139/CJPS-2014-359

    Article  Google Scholar 

  • Kim YS, Kim EK, Nawarathna W, Dong X, Shin WB, Park JS, Moon SH, Park PJ (2017) Immune-stimulatory effects of Althaea rosea flower extracts through the MAPK signaling pathway in RAW264.7. Cells\ Mol 22:679. https://doi.org/10.3390/molecules22050679

    Article  Google Scholar 

  • Kozlowski TT, Pallard SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334. https://doi.org/10.1663/0006-8101(2002)068[0270:aaarow]2

    Article  Google Scholar 

  • Landry EJ, Fuchs SJ, Bradley VL, Johnson RC (2017) The effect of cold acclimation on the low molecular weight carbohydrate composition of safflower. Heliyon 3:e00402. https://doi.org/10.1016/j.heliyon.2017.e00402

    Article  Google Scholar 

  • Li D, Xia Y, Lou J, Zhang D, Wang Z, Zhang J (2020) A comparative study between evergreen and deciduous daylily species reveals the potential contributions of winter shoot growth and leaf freezing tolerance to foliar habits. J Plant Growth Regul 39:1030–1045. https://doi.org/10.1007/s00344-019-10042-x

    Article  Google Scholar 

  • Lim CC, Arora R, Townsend EC (1998) Comparing Gompertz and Richards functions to estimate freezing injury in Rhododendron using electrolyte leakage. J Am Soc Hortic Sci 123:246–252

    Article  Google Scholar 

  • Maibam P, Nawkar G, Park J, Sahi V, Lee S, Kan C (2013) The influence of light quality, circadian rhythm, and photoperiod on the CBF-mediated freezing tolerance. Inter J Mol Sci 14:11527–11543. https://doi.org/10.3390/ijms140611527

    Article  Google Scholar 

  • Malyshev AV, Henry HAL, Kreyling J (2014) Relative effects of temperature vs. photoperiod on growth and cold acclimation of northern and southern ecotypes of the grass Arrhenatherum elatius. Environ Exp Bot 106:189–196. https://doi.org/10.1016/j.envexpbot.2014.02.007

    Article  Google Scholar 

  • Miki Y, Takahashi D, Kawamura Y, Uemura M (2018) Temporal proteomics of arabidopsis plasma membrane during cold- and deacclimation. J Proteomics 197:71–81

    Article  Google Scholar 

  • Mnich E, Bjarnholt N, Eudes A, Harholt J, Holland C, Jørgensen B, Hofmann Larsen F, Liu M, Manat R, Meyer AS, Mikkelsen JD, Motawia MS, Muschiol J, Moller BL, Moller SR, Perzon A, Petersen BL, Ravn JL, Ulvskov P (2020) Phenolic cross-links: building and de-constructing the plant cell wall. Nat Prod Rep 37:919–961. https://doi.org/10.1039/c9np00028c

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:67–880

    Google Scholar 

  • Nezami A, Bandara MS, Gusta LV (2012) An evaluation of freezing tolerance of winter chickpea (Cicer arietinum L.) using controlled freeze tests. Can J Plant Sci 92(1):155–161

    Article  Google Scholar 

  • Olennikov DN, Chirikova NK, Kashchenko NI, Gornostai TG, Selyutina IY, Zilfikarov IN (2017) Effect of low temperature cultivation on the phytochemical profile and bioactivity of arctic plants: a case of Dracocephalum palmatum. Inter Journal Mol Sci 18:2579. https://doi.org/10.3390/ijms18122579

    Article  Google Scholar 

  • Oraee A, Tehranifar A, Nezami A, Shoor M (2018) Effects of drought stress on cold hardiness of non-acclimated viola (Viola × wittrockiana “Iona Gold with Blotch”) in controlled conditions. Sci Hortic 238:98–106. https://doi.org/10.1016/j.scienta.2018.04.027

    Article  Google Scholar 

  • Ostrem L, Rapacz M, Larsen A, Dalmannsdottir S, Jørgensen M (2015) Influences of growth cessation and photoacclimation on winter survival of non-native Lolium-Festuca grasses in high-latitude regions. Environ Exp Bot 111:21–31

    Article  Google Scholar 

  • Ouyang L, Leus L, De Keyser E, Van Labeke MC (2020) Cold acclimation and deacclimation of two garden rose cultivars under controlled daylength and temperature. Front Plant Sci 11:327. https://doi.org/10.3389/fpls.2020.00327

    Article  Google Scholar 

  • Palonen P (2006) Vegetative growth, cold acclimation, and dormancy as affected by temperature and photoperiod in six red raspberry (Rubus idaeus L.) cultivars. Eur J Hortic Sci 71:1–6

    Google Scholar 

  • Palonen P, Buszard D, Donnelly D (2008) Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Plant 110:393–401. https://doi.org/10.1111/j.1399-3054.2000.1100314.x

    Article  Google Scholar 

  • Rapacz M (2002) Regulation of frost resistance during cold de-acclimation and re-acclimation in oilseed rape. a possible role of PSII redox state. Physiol Plant 115:236–243. https://doi.org/10.1034/j.1399-3054.2002.1150209.x

    Article  Google Scholar 

  • Ritonga FN, Chen S (2020) Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants 9:560. https://doi.org/10.3390/plants9050560

    Article  Google Scholar 

  • Rys M, Pociecha E, Oliwa J, Ostrowska A, Jurczyk B, Saja D, Janeczko A (2020) Deacclimation of winter oilseed rape—insight into physiological changes. Agron 10:1565–1590

    Article  Google Scholar 

  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046

    Article  Google Scholar 

  • Sarkar D, Bhowmik PC, Young-In-Kwon S (2009) Cold acclimation responses of three cool-season turfgrasses and the role of proline-associated pentose phosphate pathway. Am Soc Hortic Sci 134:210–220

    Article  Google Scholar 

  • Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570. https://doi.org/10.3389/fpls.2016.00570

    Article  Google Scholar 

  • Si T, Wang X, Zhao C, Huang M, Cai J, Zhou Q, Dai T, Jian D (2018) The role of hydrogen peroxide in mediating the mechanical wounding-induced freezing tolerance in wheat. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00327

    Article  Google Scholar 

  • Sperling O, Silva LCR, Tixier A, Théroux-Rancourt G, Zwieniecki MA (2017) Temperature gradients assist carbohydrate allocation within trees. Sci Rep 7:3265. https://doi.org/10.1038/s41598-017-03608-w

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Turan Ö, Ekmekçi Y (2011) Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures. Acta Physiol Plant 33:67–78. https://doi.org/10.1007/s11738-010-0517-7

    Article  Google Scholar 

  • Turner NC (1981) Techniques and experimental approaches for the measurement of plant water stress. Plant Soil 58:339–366

    Article  Google Scholar 

  • Valizadeh Kamran R, Toorchi M, Moghadam M, Mohammadi H (2015) The effect of cold stress on H2O2 and MDA contents in barely genotypes. J Biodivers Environ Sci 7:66–75

    Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  Google Scholar 

  • Walworth AE, Warner RM (2009) Differential cold acclimation ability of Petunia spp. Am Soc Hortic Sci 44:1219–1222. https://doi.org/10.21273/HORTSCI.44.5.1219

    Article  Google Scholar 

  • Wisniewski M, Nassuth A, Arora R (2018) Cold hardiness in trees: a mini-review. Front Plant Sci 9:1394. https://doi.org/10.3389/fpls.2018.01394

    Article  Google Scholar 

  • Yadav SK (2010) Cold stress tolerance mechanisms in plants. Rev Agronomy Sustain Develop 30:515–527. https://doi.org/10.1051/agro/2009050

    Article  Google Scholar 

  • Yamazaki T, Kawamura Y, Uemura M (2009) Extracellular freezing-induced mechanical stress and surface area regulation on the plasma membrane in cold acclimated plant cell. Plant Signal Behav 4:231–233. https://doi.org/10.4161/psb.4.3.7911

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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  1. Department of Horticultural Science and Landscape, Ferdowsi University of Mashhad, Mashhad, Iran

    Atiyeh Oraee & Ali Tehranifar

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AO performed the data acquisition and writing—original draft. AT helped in project administration, supervision, and scientifically supported.

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Correspondence to Ali Tehranifar.

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Oraee, A., Tehranifar, A. How Do Different Temperature Fluctuations Affect Alcea rosea ‘nigra’ Survival?. Iran J Sci Technol Trans Sci 46, 1135–1147 (2022). https://doi.org/10.1007/s40995-022-01330-5

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