Skip to main content
Log in

Low-temperature induced changes in the ultrastructure of maize mesophyll chloroplasts strongly depend on the chilling pattern/intensity and considerably differ among inbred and hybrid genotypes

  • Original Papers
  • Published:
Photosynthetica

Abstract

The ultrastructure and dimensions of chloroplasts in leaf mesophyll cells were quantitatively examined in three parental inbred lines of maize (Zea mays L.) and their four hybrids subjected to two types of four-week low-temperature (LT) treatment: the abrupt onset of chilling temperatures (“severe chilling”, SC) and the gradual, more moderate one (“moderate chilling”, MC). The relationship between the response of individual genotypes to one or the other type of chilling was analyzed as well as the possibility to predict the behaviour of chloroplasts in hybrids from that of their parents. Although selected parameters of chloroplast ultrastructure (e.g. volume densities of granal and intergranal thylakoids, plastoglobuli, and peripheral reticulum) and dimensions changed due to the exposure of maize plants to LT, no general pattern of such changes was found for this species due to the observed intraspecific variability. The response of some genotype to SC could not be predicted from its behaviour under MC (and vice versa) and no clear rules could be applied for the inheritance of chloroplast response to chilling in the general sense. Thus, great caution should be always taken when interpreting the results of studies aimed at the dissection of chloroplast ultrastructure as affected by LT, particularly in case such studies are made with one genotype or under one type of chilling only.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ANOVA:

analysis of variance

F1 :

the first filial generation

LT:

low temperature

MC:

moderate chilling

MeC:

mesophyll cell

SC:

severe chilling

VD:

volume density

References

  • Allen, D.J., Ort, D.R.: Impact of chilling temperatures on photosynthesis in warm-climate plants.-Trends Plant Sci. 6: 36–42, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Bongard-Pierce, D.K., Evans, M.M.S., Poethig, R.S.: Heteroblastic features of leaf anatomy in maize and their genetic regulation.-Int. J. Plant Sci. 157: 331–340, 1996.

    Article  Google Scholar 

  • Čiamporová, M., Trgiňová, I.: Ultrastructure of chloroplasts in leaves and of plastids in root tips of two maize lines differing in chilling tolerance.-Biológia (Bratislava) 51: 441–447, 1996.

    Google Scholar 

  • Čiamporová, M., Trgiňová, I.: Modifications of plant cell ultrastructure accompanying metabolic responses to low temperatures.-Biológia (Bratislava) 54: 349–360, 1999.

    Google Scholar 

  • Djebali, W., Zarrouk, M., Brouquisse, R., El Kahoui, S., Limam, F., Ghorbel, M.H., Chaibi, W.: Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes.-Plant Biol. 7: 358–368, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Du, Y.-C., Nose, A., Wasano, K.: Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species.-Plant Cell Environ. 22: 317–324, 1999.

    Article  CAS  Google Scholar 

  • Fidalgo, F., Santos, A., Santos, I., Salema, R.: Effects of long-term salt stress on antioxidant defence systems, leaf water relations and chloroplast ultrastructure of potato plants.-Ann. appl. Biol. 145: 185–192, 2004.

    Article  CAS  Google Scholar 

  • Fracheboud, Y., Haldimann, P., Leipner, J., Stamp, P.: Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.).-J. exp. Bot. 50: 1533–1540, 1999.

    Article  CAS  Google Scholar 

  • Gemel, J., Golinowski, W., Kaniuga, Z.: Low-temperature induced changes in chloroplast ultrastructure in relation to changes of Hill reaction activity, manganese and free fatty acid levels in chloroplasts of chilling-sensitive and chilling-resistant plants.-Acta Physiol. Plant. 8: 135–143, 1986.

    CAS  Google Scholar 

  • Haisel, D., Pospíšilová, J., Synková, H., Schnáblová, R., Baťková, P.: Effects of abscisic acid or benzyladenine on pigment contents, chlorophyll fluorescence, and chloroplast ultrastructure during water stress and after rehydration.-Photosynthetica 44: 606–614, 2006.

    Article  CAS  Google Scholar 

  • Holá, D., Kočová, M., Körnerová, M., Sofrová, D., Sopko, B.: Genetically based differences in photochemical activities of isolated maize (Zea mays L.) mesophyll chloroplasts.-Photosynthetica 36: 187–197, 1999.

    Article  Google Scholar 

  • Holá, D., Kočová, M., Rothová, O., Chodová, D., Mikulka, J.: The effect of low growth temperature on Hill reaction and Photosystem 1 activities in three biotypes of Kochia scoparia (L.) Schrad. with different sensitivity to atrazine and ALS-inhibiting herbicides.-Plant Soil Environ. 50: 10–17, 2004.

    Google Scholar 

  • Holá, D., Kočová, M., Rothová, O., Wilhelmová, N., Benešová, M.: Recovery of maize (Zea mays L.) inbreds and hybrids from chilling stress of various duration: photosynthesis and antioxidant enzymes.-J. Plant Physiol. 164: 868–877, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Holá, D., Langrová, K., Kočová, M., Rothová, O.: Photosynthetic parameters of maize (Zea mays L.) inbred lines and F1 hybrids: their different response to, and recovery from rapid or gradual onset of low-temperature stress.-Photosynthetica 41: 429–442, 2003.

    Article  Google Scholar 

  • Holzinger, A., Buchner, O., Luetz, C., Hanson, M.R.: Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana.-Protoplasma 230: 23–30, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Hudák, J., Salaj, J.: Effect of low temperatures on the structure of plant cells.-In: Pessarakli, M. (ed.): Handbook of Plant and Crop Stress. 2nd Ed. Pp. 441–464. Marcel Dekker, New York-Basel 1999.

    Google Scholar 

  • Jagels, R.: Photosynthetic apparatus in Selaginella. II. Changes in plastid ultrastructure and pigment content under different light and temperature regimes.-Can. J. Bot. 48: 1853–1860, 1970.

    Article  CAS  Google Scholar 

  • Khavari-Nejad, R.A., Mostofi, Y.: Effects of NaCl on photosynthetic pigments, saccharides, and chloroplast ultrastructure in leaves of tomato cultivars.-Photosynthetica 35: 151–154, 1998.

    Article  CAS  Google Scholar 

  • Kimball, S.L., Salisbury, F.B.: Ultrastructural changes of plants exposed to low temperatures.-Amer. J. Bot. 60: 1028–1033, 1973.

    Article  Google Scholar 

  • Körnerová, M., Holá, D.: The effect of low growth temperature on Hill reaction and photosystem 1 activities and pigment contents in maize inbred lines and their F1 hybrids.-Photosynthetica 37: 477–488, 1999.

    Article  Google Scholar 

  • Kratsch, H.A., Wise, R.R.: The ultrastructure of chilling stress.-Plant Cell Environ. 23: 337–350, 2000.

    Article  CAS  Google Scholar 

  • Kutík, J., Holá, D., Kočová, M., Rothová, O., Haisel, D., Wilhelmová, N., Tichá, I.: 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, 2004.

    Article  Google Scholar 

  • Kutík, J., Kočová, M., Holá, D., Körnerová, M.: The development of chloroplast ultrastructure and Hill reaction activity during leaf ontogeny in different maize (Zea mays L.) genotypes.-Photosynthetica 36: 497–507, 1999.

    Article  Google Scholar 

  • Ladygin, V.G.: Composition of complexes, activity of photosystems and architecture of chloroplast membranes in leaves of Pisum sativum at iron deficit and root anoxia.-Biol. Membr. 20: 451–463, 2003.

    CAS  Google Scholar 

  • Ladygin, V.G.: Photochemical activity, spectral properties, and structure of chloroplasts in leaves of Pisum sativum L. under iron deficit and root anaerobiosis.-Biofizika 50: 86–100, 2005.

    PubMed  CAS  Google Scholar 

  • Li, W.X., Chen, T.B., Huang, Z.C., Lei, M., Liao, X.Y.: Effect of arsenic on chloroplast ultrastructure and calcium distribution in arsenic hyperaccumulator Pteris vittata L.-Chemosphere 62: 803–809, 2006.

    Article  PubMed  CAS  Google Scholar 

  • McCain, D.C.: Combined effects of light and water stress on chloroplast volume regulation.-Biophys. J. 69: 1105–1110, 1995.

    PubMed  CAS  Google Scholar 

  • Murphy, C., Wilson, J.M.: Ultrastructural features of chilling injury in Episcia reptans.-Plant Cell Environ. 4: 261–265, 1981.

    Google Scholar 

  • Musser, R.L., Thomas, S.A., Wise, R.R., Peeler, T.C., Naylor, A.W.: Chloroplast ultrastructure, chlorophyll fluorescence, and pigment composition in chilling stressed soybeans.-Plant Physiol. 74: 749–754, 1984.

    PubMed  CAS  Google Scholar 

  • Papadakis, I.E., Giannakoula, A., Therios, I.N., Bosabalidis, A.M., Moustakas, M., Nastou, A.: Mn-induced changes in leaf structure and chloroplast ultrastructure of Citrus volkameriana (L.) plants.-J. Plant Physiol. 164: 100–103, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Pechová, R., Kutík, J., Holá, D., Kočová, M., Haisel, D., Vičánková, A.: The ultrastructure of chloroplasts, content of photosynthetic pigments, and photochemical activity of maize (Zea mays L.) as influenced by different concentrations of the herbicide amitrole.-Photosynthetica 41: 127–136, 2003.

    Article  Google Scholar 

  • Pinhero, R.G., Paliyath, G., Yada, R.Y., Murr, D.: Chloroplast membrane organization in chilling-tolerant and chilling-sensitive maize seedlings.-J. Plant Physiol. 155: 691–698, 1999.

    CAS  Google Scholar 

  • Ristic, Z., Cass, D.D.: Chloroplast structure after water and high-temperature stress in two lines of maize that differ in endogenous levels of abscisic acid.-Int. J. Plant Sci. 153: 186–196, 1992.

    Article  CAS  Google Scholar 

  • Semenova, G.A.: Structural reorganization of thylakoid systems in response to heat treatment.-Photosynthetica 42: 521–527, 2004.

    Article  Google Scholar 

  • Sharkova, V.E., Bubolo, L.S.: Effect of heat stress on the arrangement of thylakoid membranes in the chloroplasts of mature wheat leaves.-Russ. J. Plant Physiol. 43: 358–365, 1996.

    CAS  Google Scholar 

  • Smillie, R.M., Critchley, C., Bain, J.M., Nott, R.: Effect of growth temperature on chloroplast structure and activity in barley.-Plant Physiol. 62: 191–196, 1978.

    PubMed  CAS  Google Scholar 

  • Sowinski, P., Rudzinska-Langwald, A., Adamczyk, J., Kubica, W., Fronk, J.: Recovery of maize seedling growth, development and photosynthetic efficiency after initial growth at low temperature.-J. Plant Physiol. 162: 67–80, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, A.O., Craig, A.S.: Plants under climatic stress. II. Low temperature, high light effects on chloroplast ultrastructure.-Plant Physiol. 47: 719–725, 1971.

    Article  PubMed  Google Scholar 

  • Vani, B., Saradhi, P.P., Mohanty, P.: Alteration in chloroplast structure and thylakoid membrane composition due to in vivo heat treatment of rice seedlings: correlation with the functional changes.-J. Plant Physiol. 158: 583–592, 2001.

    Article  CAS  Google Scholar 

  • Vega, S.H., Sauer, M., Orkwiszewski, J.A.J., Poethig, R.S.: The early phase change gene in maize.-Plant Cell 14: 133–147, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Weibel, E.R.: Stereological Methods. Vol. 1. Practical Methods for Biological Morphometry.-Academic Press, London 1979.

    Google Scholar 

  • Wheeler, W.S., Fagerberg, W.R.: Exposure to low levels of photosynthetically active radiation induces rapid increases in palisade cell chloroplast volume and thylakoid surface area in sunflower (Helianthus annuus L.).-Protoplasma 212: 38–45, 2000.

    Article  Google Scholar 

  • Wise, R.R., McWilliam, J.R., Naylor, A.W.: A comparative study of low-temperature-induced ultrastructural alterations of three species with different chilling sensitivities.-Plant Cell Environ. 6: 525–535, 1983.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Xu, S., Li, J.L., Zhang, X.Q., Wei, H., Cui, L.J.: Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress.-Environ. exp. Bot. 56: 274–285, 2006.

    Article  CAS  Google Scholar 

  • Yamane, K., Hayakawa, K., Kawasaki, M., Taniguchi, M., Miyake, H.: Bundle sheath chloroplasts of rice are more sensitive to drought stress than mesophyll chloroplasts.-J. Plant Physiol. 160: 1319–1327, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Yamane, K., Rahman, M.S., Kawasaki, M., Taniguchi, M., Miyake, H.: Pretreatment with a low concentration of methyl viologen decreases the effects of salt stress on chloroplast ultrastructure in rice leaves (Oryza sativa L.).-Plant Product. Sci. 7: 435–441, 2004.

    Article  CAS  Google Scholar 

  • Zellnig, G., Zechmann, B., Perktold, A.: Morphological and quantitative data of plastids and mitochondria within drought-stressed spinach leaves.-Protoplasma 223: 221–227, 2004.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Holá.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holá, D., Kutík, J., Kočová, M. et al. Low-temperature induced changes in the ultrastructure of maize mesophyll chloroplasts strongly depend on the chilling pattern/intensity and considerably differ among inbred and hybrid genotypes. Photosynthetica 46, 329–338 (2008). https://doi.org/10.1007/s11099-008-0061-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-008-0061-5

Additional key words

Navigation