Skip to main content
SpringerLink
Log in

The effect of abscisic acid on cold tolerance and chloroplasts ultrastructure in wheat under optimal and cold stress conditions

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The effect of abscisic acid (0.1 mM) on cold tolerance of leaf cells and ultrastructure of chloroplasts in wheat (Triticum aestivum L.) under optimal (22 °C) and cold stress conditions (4 °C) was studied. Results indicated that exogenous abscisic acid induces a rise in the cold tolerance of wheat along with a number of significant ultrastructural changes in chloroplasts both at 22 and at 4 °C. Some of them (increase in density of chloroplasts stroma, formation of “distorted” and “dilated” thylakoids, appearance of invaginations, changes in the shape of chloroplasts and increase of their dimension owing to the stroma area) were common to the two types of treatments. At the same time, the character of changes in the membrane system of plastids was temperature specific, i.e. if at 22 °C the hormone caused a considerable increase in the length of photosynthetic membranes in chloroplast owing the length of both appressed and non-appressed membranes of thylakoids, then in cold stress conditions observed an increase in the number of grana and the length of appressed membranes of thylakoids. These results suggested that the rise in the cold tolerance of abscisic acid-treated plants is associated with the ultrastructural reorganization of chloroplasts aimed to defense plant cells against chilling injury and to maintain the activity of the photosynthetic system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akter K, Kato M, Sato Y, Kaneco Y, Takezawa D (2014) Abscisic acid-induced rearrangement of intracellular structures associated with freezing and desiccation tress tolerance in the liverwort Marchantia polymorpha. J Plant Physiol 171:1334–1343

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Vernieri P, Irigoyen JJ, Sánchez-Diaz M, Tognoni F, Pardossi A (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165:671–679

    Article  CAS  Google Scholar 

  • Asthir B, Kaur S, Mann SK (2009) Effect of salicylic and abscisic acid administered through detached tiller on antioxidand system in developing wheat grains under heat stress. Acta Physiol Plant 31:1091–1109

    Article  CAS  Google Scholar 

  • Badowiek A, Świgonska S, Szypulka E, Weidner S (2012) Influence of exogenous abscisic acid on alterations in protein expression in the proteome of Triticosecale seedlings. Acta Physiol Plant 6(34):2359–2368

    Article  Google Scholar 

  • Bakht J, Bano A, Dominy P (2006) The role of abscisic acid and low temperature in in chickpea (Cicer arientum) cold tolerance. II. Effect on plasma membrane structure and function. J Exp Bot 57:3707–3715

    Article  CAS  PubMed  Google Scholar 

  • Bohn M, Lüthje S, Sperling P, Heinz E, Dörffling K (2007) Plasma membrane lipid alterations induced by cold acclimation and abscisic acid treatment of winter wheat seedlings differing in frost resistance. J Plant Physiol 164:146–156

    Article  CAS  PubMed  Google Scholar 

  • Catalá R, Salinas J (2010) Temperature-perception, molecules and mechanisms. J Appl Biomed 8:189–198

    Article  Google Scholar 

  • Chen WP, Li PH (2002) Membrane stabilization by abcsicic acid under cold aids proline in alleviating chilling injury in maize (Zea mays L.). Plant Cell Environ 25:955–962

    Article  CAS  Google Scholar 

  • Chono M, Matsunaka H, Seki M, Fujita M, Kiribuchi-Otobe C, Oda S, Kojima H, Kobayashi D, Kawakami N (2013) Isolation of a wheat (Triticum aestivum L.) mutant in ABA 8′-hydroxylase gene: effect of reduced ABA catabolism on germination inhibition under field condition. Breed Sci 63:104–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corrêa de Souza T, Magalhães PC, Mauro de Castro E, Pereira de Albuquerque PE, Marabesi MA (2013) The influence of ABA on water relation, photosynthesis parameters, and chlorophyll fluorescence under drought conditions in two maize hybrids with contrasting drought resistance. Acta Physiol Plant 35:515–527

    Article  Google Scholar 

  • Crosatti C, Rizza F, Badeck FW, Mazzucotelli E, Cattivelli L (2013) Harden the chloroplast to protect the plant. Physiol Plant 147:55–63

    Article  CAS  PubMed  Google Scholar 

  • Dallaire S, Houde M, Gagné Y, Saini HS, Boileau S, Chevrier N, Sarhan F (1994) ABA and low temperature induce freezing tolerance via distinct regulatory pathways in wheat. Plant Cell Physiol 35:1–9

    CAS  Google Scholar 

  • Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Flores-Nimedes AA, Dörffling K, Vergara BS (1993) Improvement of chilling resistance in rice by application of an abscisic acid analog in combination with the growth retardant tetcyclacis. J Plant Growth Regul 12:27–34

    Article  Google Scholar 

  • Garbero M, Pedranzani H, Zirulnik F, Molina A, Péres-Chaca MV, Vigliocco A, Abdala G (2011) Short-term cold stress in two cultivars of Digitaria eriantha: effects on stress-related hormones and antioxidant defense system. Acta Physiol Plant 33:497–507

    Article  CAS  Google Scholar 

  • Garbero M, Andrade A, Reinoso H, Fernández B, Cuesta C, Granda V, Escudero C, Abdala G, Pedranzani H (2012) Differential effect of short-term cold stress on growth, anatomy, and hormone levels in cold-sensitive versus resistance cultivars of Digiteria eriantha. Acta Physiol Plant 34:2079–2091

    Article  CAS  Google Scholar 

  • Goral TK, Johnson MP, Duffy CD, Brain PR, Ruban AV (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membrane in Arabidopsis. Plant J 69:289–301

    Article  CAS  PubMed  Google Scholar 

  • Gray CG, Hansen MR, Shau DJ, Graham K, Dale R, Natesan SKA, Newell CA (2012) Plastid stromules are induced by stress treatments acting through abscisic acid. Plant J 69:387–398

    Article  CAS  PubMed  Google Scholar 

  • Guo WL, Chen RG, Gong ZH, Yin YX, Ahmed SS, He YM (2012) Exogenous abscisic acid increases antioxidant enzymes and related gene expression in pepper (Capsicum annuum) leaves subjected to chilling stress. Genet Mol Res 11:4063–4080

    Article  CAS  PubMed  Google Scholar 

  • Guóth A, Benyó D, Csiszár J, Gallé Á, Horváth F, Cseur L, Erdey L, Tari I (2010) Relatioship between osmotic stress-induced abscisic acid accumulation, biomass production and plant growth in drought-tolerance and -sensitive wheat cultivars. Acta Physiol Plant 32:719–727

    Article  Google Scholar 

  • Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of abscisic acid. J Plant Growth Regul 24:308–318

    Article  CAS  Google Scholar 

  • Heidarvand L, Amiri M (2010) What happens in plant molecules responses to cold stress. Acta Physiol Plant 32:419–431

    Article  CAS  Google Scholar 

  • Huner NPM, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:1360–1385

    Article  Google Scholar 

  • Janmohammadi M, Enayati V, Sabaghnia N (2012) 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

    Google Scholar 

  • Khatoon M, Inagawa K, Pospisil P, Yamashita A, Yoshioka M, Lundin B, Horie J, Morita N, Yamamoto Y, Yamamoto Y (2009) Quality control of photosystem II thylakoid unstacking is necessary to avoid further damage to the D1 protein and to facilitate D1 degradation under light stress in spinach thylakoids. J Biol Chem 284:25343–25352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klíma M, Vítámvás P, Selenková S, Vyvadilová M, Prášil IT (2012) Dehydrin and proline content in Brassica napus and B. carinata under cold stress at two irradiances. Biol Plant 56:157–161

    Article  Google Scholar 

  • Kobayashi F, Takumi S, Nakamura C (2008) Increased freezing tolerance in an ABA-hypersensitive mutant of common wheat. J Plant Physiol 165:224–232

    Article  CAS  PubMed  Google Scholar 

  • Koleva D, Ganeva Ts, Stefanova M (2013) Effect of ABA pretreatment on chloroplast structure in Hypericum rumeliacum Boiss. plants subjected to cryopreservation. Bulg J Agric Sci 19:18–21

    Google Scholar 

  • Kovács Z, Simon-Sarcadi L, Szűcz A, Kocsy G (2010) Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids 38:623–631

    Article  PubMed  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • Kutik J, Hola D, Kocova M, Rothova O, Haise D, Wilhelmova N, Ticha I (2004) Ultrastructure and dimensions of chloroplasts in leaves of three maize (Zea mays L.) inbred lines and their F1 hybrids grown under moderate chilling stress. Photosynthetica 42:447–455

    Article  Google Scholar 

  • Liu F, Jensen CR, Andersen MN (2005) A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-dased chemical signals. Aust J Agric Res 56:1245–1252

    Article  CAS  Google Scholar 

  • Mäntylä E, Lång V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LTI78 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148

    PubMed  PubMed Central  Google Scholar 

  • Morillon R, Chrispeels MJ (2001) The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc Natl Acad Sci USA 98:14138–14143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • Nayyar H, Walia DP (2003) Water stress induced proline accumulation in contrasting wheat genotypes as affected by calcium and abscisic acid. Biol Plant 46:275–279

    Article  CAS  Google Scholar 

  • Pastorczyk M, Gielwanowska I, Lahuta LB (2014) Changes in soluble carbohydrates in polar Caryophyllaceae and Poaceae plants in response to chilling. Acta Physiol Plant 36:1771–1780

    Article  CAS  Google Scholar 

  • Pribil M, Labs M, Leister D (2014) Structure and dynamics of thylakoids in land plants. J Exp Bot 65:1955–1972

    Article  CAS  PubMed  Google Scholar 

  • Qin F, Shinozaki K, Yamaguchi- Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582

    Article  CAS  PubMed  Google Scholar 

  • Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434

    Article  CAS  PubMed  Google Scholar 

  • Roychoundhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006

    Article  Google Scholar 

  • Ruelland E, Zachowsky A (2010) How plant sense temperature. Environ Exp Bot 69:225–232

    Article  Google Scholar 

  • Saibo NJ, Lourenço T, Oliveria MM (2009) Transcription factors and regulation of photosynthesis and related metabolism under environmental stresses. Ann Botany 103:609–623

    Article  CAS  Google Scholar 

  • Shakirova FM, Bezrukova MV, Shayakhmetov IF (1996) Effect of temperature shock on the dynamics of abscisic acid and wheat germ agglutinin accumulation in wheat cell culture. Plant Growth Regul 19:85–87

    Article  CAS  Google Scholar 

  • Talanova VV, Titov AF, Topchieva LV, Malysheva IE, Venzhik YuV, Frolova SA (2009) Expression of WRKY transcription factor and stress protein genes in wheat plants during cold hardening and ABA treatment. Russ J Plant Physiol 56:702–708

    Article  CAS  Google Scholar 

  • Teng K, Li J, Liu L, Han Y, Du Y, Zhang J, Sun H, Zhao Q (2014) Exogenous ABA induced drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiol Plant 36:2219–2227

    Article  CAS  Google Scholar 

  • Titov AF, Talanova VV, Akimova TV (2003) The effect of root treatment with various stress agents on plant cold- and heat tolerance. Russ J Plant Physiol 50:94–99

    Article  Google Scholar 

  • Travaglia C, Cohen AC, Reinoso H, Castillo C, Bottini R (2007) Exogenous abscisic acid increases carbohydrate accumulation and redistribution to the grains in wheat grown under field conditions os soil water restriction. J Plant Growth Regul 26:285–289

    Article  CAS  Google Scholar 

  • Tsuda K, Tsvetanov S, Takumi S, Mor N, Atanassov A, Nakamura C (2000) New members of a cold-responsive Group-3 Lea/Rab-related Cor gene family from common wheat (Triticum aestivum L.). Gen Genet Syst 75:179–188

    Article  CAS  Google Scholar 

  • Venzhik YV, Titov A, Talanova VV, Miroslavov EA, Koteeva NK (2013) Structural and functional reorganization of the photosynthetic apparatus in adaptation to cold of wheat plants. Cell Tissue Biol 7:168–176

    Article  Google Scholar 

  • Venzhik YV, Titov AF, Talanova VV, Miroslavov EA (2014) Ultrastructure and functional activity of chloroplasts in wheat leaves under root chilling. Acta Physiol Plant 36:323–330

    Article  CAS  Google Scholar 

  • Wang T, Zhang X, Li C (2007) Growth, abscisic acid content, and carbon isotope composition in wheat cultivars grown under different soil moisture. Biol Plant 51:181–184

    Article  CAS  Google Scholar 

  • Wang G-L, Miao W, Wang JY, Ma D-R, Li J-Q, Chen W-F (2013) Effect of exogenous abscisic acid on antioxidant system in weedy and cultivated rice with different chilling sensitivity under chilling stress. J Agron Crop Sci 199:200–208

    Article  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signaling: the coordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Lightner J, Warwick N, Browse J (1997) Low-temperature damage and subsequent recovery of fab1 mutant Arabidopsis exposed to 2 °C. Plant Physiol 113:347–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto Y, Kai S, Ohnishi A, Tsumura N, Ishikawa T, Hori H, Morita N, Ishikawa Y (2014) Quality control of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol 55:1206–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamburenko MV, Zubo YO, Vanková R, Kusnetsov VV, Kulaeva ON, Börner T (2013) Abscisic acid represses the transcription of chloroplast genes. J Exp Bot 64:4491–4502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Jia W, Yang J (2004) ABA in plant water stress signaling. Proc Indian Natl Sci Acad 70:367–377

    CAS  Google Scholar 

  • Zhou B, Guo Z, Lin L (2006) Effects of abscisic acid application on photosynthesis and photochemistry of Stylosanthes guianensis under chilling stress. Plant Growth Regul 48:195–199

    CAS  Google Scholar 

Download references

Acknowledgments

The study was carried out under state order (project No. 0221-2014-0002).

Author information

Authors and Affiliations

  1. Institute of Biology, Karelian Research Centre, Russian Academy of Sciences, Petrozavodsk, Russian Federation

    Yuliya Venzhik, Vera Talanova & Alexandr Titov

Authors
  1. Yuliya Venzhik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vera Talanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandr Titov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuliya Venzhik.

Additional information

Communicated by H Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Venzhik, Y., Talanova, V. & Titov, A. The effect of abscisic acid on cold tolerance and chloroplasts ultrastructure in wheat under optimal and cold stress conditions. Acta Physiol Plant 38, 63 (2016). https://doi.org/10.1007/s11738-016-2082-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2082-1

Keywords

Search

Navigation