biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 51:690-698, 2007 | DOI: 10.1007/s10535-007-0144-3

Ultrastructural alterations in mesophyll and bundle sheath chloroplasts of two maize cultivars in response to chilling at high irradiance

A. S. Saropulos1,*, D. S. H. Drennan1
1 Department of Agricultural Botany, the University of Reading, Reading, UK

Maize (Zea mays L.) seedlings of two cultivars (cv. Bastion adapted to W. Europe, and cv. Batan 8686 adapted to the highlands of Mexico), raised in a glasshouse (19-25 °C), were transferred to 4.5 or 9 °C at photon flux density (PPFD) of 950 µmol m-2 s-1 with 10-h photoperiod for 58 h and then allowed to recover at 22 °C for 16 h (14 h dark and 2 h at PPFD of 180 µmol m-2 s-1). The ultrastructural responses after 4 h or 26 h at 4.5 °C were the disappearance of starch grains in the bundle sheath chloroplasts and the contraction of intrathylakoid spaces in stromal thylakoids of the mesophyll chloroplasts. At this time, bundle sheath chloroplasts of cv. Batan 8686 formed peripheral reticulum. Prolonged stress at 4.5 °C (50 h) caused plastid swelling and the dilation of intrathylakoid spaces, mainly in mesophyll chloroplasts. Bundle sheath chloroplasts of cv. Batan 8686 seedlings appeared well preserved in shape and structure. Batan 8686 had also higher net photosynthetic rates during chilling and recovery than Bastion. Extended leaf photobleaching developed during the recovery period after chilling at 4.5 °C. This was associated with collapsed chloroplast envelopes, disintegrated chloroplasts and very poor staining.

Keywords: low temperature; photooxidation; photosynthesis; Zea mays
Subjects: bundle sheath; chloroplast, chilling; chloroplast ultrastructure; cultivar and genotype differences; gas exchange; maize; photon flux density (PPFD, PFD); Zea mays

Received: November 23, 2005; Accepted: August 8, 2006; Published: December 1, 2007  Show citation

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Saropulos, A.S., & Drennan, D.S.H. (2007). Ultrastructural alterations in mesophyll and bundle sheath chloroplasts of two maize cultivars in response to chilling at high irradiance. Biologia plantarum51(4), 690-698. doi: 10.1007/s10535-007-0144-3
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References

  1. Baker, N.R., Long, S.P., Ort, D.R.: Photosynthesis and temperature, with particular reference to effects on quantum yield.-In: Long, S.P., Woodward, F.I. (ed.): Plants and Temperature. Pp. 347-375. The Company of Biologists Limited, Cambridge 1988.
  2. Baker, N.R., Nie, G.Y.: Chilling sensitivity of photosynthesis in maize.-In: Bajaj, Y.P.S. (ed.): Biotechnology in Agriculture and Forestry: Maize. Vol. 9. Pp. 465-481. Springer-Verlag, Berlin 1994. Go to original source...
  3. Bonner, L.J.: Pollination Biology of Lycopersicon esculentum Mill. in Summer and Winter.-PhD Thesis. The University of Reading, Reading 1988.
  4. Doulis, A.G., Debian, N., Kingston-Smith, A.H., Foyer, C.H.: Differential localization of antioxidants in maize leaves.-Plant Physiol. 114: 1031-1037, 1997. Go to original source...
  5. Fryer, M.J., Andrews, J.R., Oxborough, K., Blowers, D.A., Baker, N.R.: Relationship between CO2 assimilation, photosynthetic electron transport and active O2 metabolism in leaves of maize in the field during periods of low temperature.-Plant Physiol. 116: 571-580, 1998. Go to original source...
  6. Giles, K.L., Beardsell, M.F., Cohen, D.: Cellular and ultrastructural changes in mesophyll and bundle sheath cells of maize in response to water stress.-Plant Physiol. 54: 208-212, 1974. Go to original source...
  7. Gomez, L.D., Vanacker, H., Buchner, P., Noctor, G., Foyer, C.H.: Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling.-Plant Physiol. 134: 1662-1671, 2004. Go to original source...
  8. Haldimann, P.: How do changes in temperature during growth affect leaf pigment composition and photosynthesis in Zea mays genotypes differing in sensitivity to low temperature?-J. exp. Bot. 50: 543-550, 1999. Go to original source...
  9. Halliwell, B. (ed.): Chloroplast Metabolism: The Structure and Function of Chloroplasts in Green Leaf Cells.-Clarendon Press, Oxford 1984.
  10. Hatch, M.D.: C4 pathway photosynthesis: mechanism and physiological function.-Trends Biochem. Sci. 2: 199-201, 1977. Go to original source...
  11. Huang, M., Guo, Z.: Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity.-Biol. Plant. 49: 81-84, 2005. Go to original source...
  12. Jatimliansky, J.R., García, M.D., Molina, M.C.: Response to chilling of Zea mays, Tripsacum dactyloides and their hybrid.-Biol. Plant. 48: 561-567, 2004. Go to original source...
  13. Kingston-Smith, A.H., Foyer, C.H.: Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures.-J. exp. Bot. 51: 123-130, 2000. Go to original source...
  14. Kramer, D.M., Sacksteder, C.A., Cruz, J.A.: How acidic is the lumen?-Photosynth. Res. 60: 151-163, 1999. Go to original source...
  15. Kratsch, H.A., Wise, R.R.: The ultrastructure of chilling stress.-Plant Cell Environ. 23: 337-350, 2000. Go to original source...
  16. Kutík, J., Holá, D., Kočová, M., Rothová, O., Haisel, D., Wilhelmová, N., Tichá, I.: The 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. Go to original source...
  17. Laetsch, W.M.: The C4 syndrome: A structural analysis.-Annu. Rev. Plant Physiol. 25: 27-52, 1974. Go to original source...
  18. Long, S.P., Humphries, S., Falkowski, P.G.: Photoinhibition of photosynthesis in nature.-Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 633-662, 1994. Go to original source...
  19. Ma, S., Lin, C., Chen, Y.: Comparative studies of chilling stress on alterations of chloroplast ultrastructure and protein synthesis in the leaves of chilling-sensitive (mungbean) and-insensitive (pea) seedlings.-Bot. Bull. Acad. sin. 31: 263-272, 1990.
  20. Murakami, S., Packer, L.: Light-induced changes in the conformation and configuration of the thylakoid membrane of Ulva and Porphyra chloroplasts in vivo.-Plant Physiol. 45: 289-299, 1970a. Go to original source...
  21. Murakami, S., Packer, L.: Protonation and chloroplast membrane structure.-J. Cell Biol. 47: 332-351, 1970b. Go to original source...
  22. Murphy, C., Wilson, J.M.: Ultrastructural features of chilling-injury in Episcia reptans.-Plant Cell Environ. 4: 261-265, 1981. Go to original source...
  23. 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. Go to original source...
  24. Pastori, G., Foyer, C.H., Mullineaux, P.: Low temperature-induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves.-J. exp. Bot. 51: 107-113, 2000. Go to original source...
  25. Pinhero, R.G., Paliyath, G., Yada, R.Y., Murr, D.P.: Chloroplast membrane organization in chilling-tolerant and chilling-sensitive maize seedlings.-J. Plant Physiol. 155: 691-698, 1999. Go to original source...
  26. Saropulos, A.S.: Chilling-induced Physiological Dysfunction in Leaves of Zea mays L. and Capsicum annuum L. Seedlings.-PhD Thesis. The University of Reading, Reading 1995.
  27. Saropulos, A.S., Drennan, D.S.H: Leaf photosynthetic parameters of two maize (Zea mays L.) cultivars in response to various patterns of chilling temperatures and photon flux densities.-Ann. appl. Biol. 141: 237-245, 2002. Go to original source...
  28. Slack, C.R., Roughan, P.G., Bassett, H.C.M.: Selective inhibition of mesophyll chloroplast development in some C4-pathway species by low night temperature.-Planta 118: 57-73, 1974. Go to original source...
  29. Sopher, C.R., Krol, M., Huner, N.P.A., Moore, A.E., Fletcher, R.A.: Chloroplastic changes associated with paclobutrazol-induced stress protection in maize seedlings.-Can. J. Bot. 77: 279-290, 1999. Go to original source...
  30. 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. Go to original source...
  31. Tevini, M., Steinmüller, D.: Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beech leaf senescence.-Planta 163: 91-96, 1985. Go to original source...
  32. Von Caemmerer, S., Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.-Planta 153: 376-387, 1981. Go to original source...
  33. Wise, R.R.: Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light.-Photosynth. Res. 45: 79-97, 1995. Go to original source...
  34. Wise, R.R., Cook, W.B.: Development of ultrastructural damage to chloroplasts in a plastoquinone-deficient mutant of maize.-Environ. exp. Bot. 40: 221-228, 1998. Go to original source...
  35. Wise, R.R., Naylor, A.W.: Chilling-enhanced photooxidation. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure.-Plant Physiol. 83: 272-277, 1987. Go to original source...
  36. Wise, R.R., McWilliam, J.R., Naylor, A.W.: A comparative study of low-temperature-induced ultrastructural alterations of three species with differing chilling sensitivities.-Plant Cell Environ. 6: 525-535, 1983. Go to original source...