Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming

Protoplasma

Volumn 249, Issue 4, 2012, Pages 1137-1149

  Vella, Nicole G F ^a   Joss, Tom V ^a   Roberts, Thomas H ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Arabidopsis; Chloroplast; Mesophyll; Mitochondrion; Thylakoids; Ultrastructure

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84867139901     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-011-0363-5     Document Type: Article

References (70)

1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with Image. J Biophotonics Int 11: 36-42.
2. Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6: 36-42.
3. Arimura S, Fujimoto M, Doniwa Y, Kadoya N, Nakazono M, Sakamoto W, Tsutsumi N (2008) Arabidopsis ELONGATED MITOCHONDRIA1 is required for localization of DYNAMIN-RELATED PROTEIN3A to mitochondrial fission sites. Plant Cell 20: 1555-1566.
4. Armstrong AF, Logan DC, Atkin OK (2006a) On the developmental dependence of leaf respiration: responses to short- and long-term changes in growth temperature. Am J Bot 93: 1633-1639.
5. Armstrong AF, Logan DC, Tobin AK, O'Toole P, Atkin OK (2006b) Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant Cell Environ 29: 940-949.
6. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8: 343-351.
7. Bereiter-Hahn J, Voth M (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech 27: 198-219.
8. Berndt M-L, McCully ME, Canny MJ (1999) Is xylem embolism and refilling involved in the rapid wilting and recovery of plants following root cooling and rewarming? Plant Biol 1: 506-515.
9. Capell B, Dorffling K (2006) Genotype-specific differences in chilling tolerance of maize in relation to chilling-induced changes in water status and abscisic acid accumulation. Physiol Plant 88: 638-646.
10. Fujimoto M, Arimura S, Mano S, Kondo M, Saito C, Ueda T, Nakazono M, Nakano A, Nishimura M, Tsutsumi N (2009) Arabidopsis dynamin-related proteins DRP3A and DRP3B are functionally redundant in mitochondrial fission, but have distinct roles in peroxisomal fission. Plant J 58: 388-400.
11. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058.
12. Ghadially FN (1988) Ultrastructure pathology of the cell and matrix. Butterworths, London.
13. Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17: 1233-1240.
14. Gilmour SJ, Hajela RK, Thomashow MF (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiol 87: 745-750.
15. Gorsuch PA, Pandey S, Atkin OK (2010a) Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves. Plant Cell Environ 33: 244-258.
16. Gorsuch PA, Pandey S, Atkin OK (2010b) Thermal de-acclimation: how permanent are leaf phenotypes when cold-acclimated plants experience warming? Plant Cell Environ 33: 1124-1137.
17. Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132: 220-235.
18. Henriques R, Lelek M, Fornasiero EF, Valtorta F, Zimmer C, Mhlanga MM (2010) QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat Methods 7: 339-340.
19. Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98: 1105-1114.
20. Hurry VM, Huner NP (1991) Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. Plant Physiol 96: 491-497.
21. Hurry VM, Huner NP (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol 100: 1283-1290.
22. Ilker R, Waring AJ, Lyons JM, Breidenback RW (1976) The cytological responses of tomato-seedling cotyledons to chilling and the influence of membrane modifications upon these responses. Protoplasma 90: 229-252.
23. Ishikawa HA (1996) Ultrastructural features of chilling injury: injured cells and the early events during chilling of suspension-cultured mung bean cells. Am J Bot 83: 825-835.
24. Ishitani M, Xiong L, Stevenson B, Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9: 1935-1949.
25. Jagels R (1970) Photosynthetic apparatus in Selaginella. II. Changes in plastid ultrastructure and pigment content under different light and temperature regimes. Can J Bot 48: 1853-1860.
26. Kaplan F, Guy CL (2004) Beta-amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135: 1674-1684.
27. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-743.
28. Kawata T, Yoshida S (1988) Alterations in protein synthesis in vivo in chilling-sensitive mung bean hypocotyls caused by chilling stress. Plant Cell Physiol 29: 1423-1427.
29. Kirk JTO, Tilney-Bassett RAE (1978) The plastids: their chemistry, structure, growth and inheritance. Elsevier, North Holland.
30. Kislyuk IM (1963) Morphological and functional changes of chloroplasts after cooling of leaves of Cuminis sativus L. In: Troshin AS (ed) The cell and environmental temperature. Pergamon Press, London, pp 59-63.
31. Klein S (1960) The effect of low temperature on the development of the lamellar system in chloroplasts. J Biophys Biochem Cytol 8: 529-538.
32. Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23: 337-350.
33. Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14: 1235-1251.
34. Leheny EA, Theg SM (1994) Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations not membrane fluidity. Plant Cell 6: 427-437.
35. Li XP, Ong BL (1997) Ultrastructural changes in gametophytes of Acrostichum aureum L. cultured in different sodium chloride concentrations. Biol Plant 39: 607-614.
36. Li L, Ilarslan H, James MG, Myers AM, Wurtele ES (2007) Genome wide co-expression among the starch debranching enzyme genes AtISA1, AtISA2, and AtISA3 in Arabidopsis thaliana. J Exp Bot 58: 3323-3342.
37. Li TA, Xu SL, Oses-Prieto JA, Putil S, Xu P, Wang RJ, Li KH, Maltby DA, An LH, Burlingame AL, Deng ZP, Wang ZY (2011) Proteomics analysis reveals post-translational mechanisms for cold-induced metabolic changes in Arabidopsis. Mol Plant 4: 361-374.
38. Logan DC (2006) Plant mitochondrial dynamics. Biochim Biophys Acta 1763: 430-441.
39. Logan DC (2010) Mitochondrial fusion, division and positioning in plants. Biochem Soc Trans 38: 789-795.
40. Logan DC, Leaver CJ (2000) Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. J Exp Bot 51: 865-871.
41. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24: 445-466.
42. Mano S, Nakamori C, Kondo M, Hayashi M, Nishimura M (2004) An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J 38: 487-498.
43. Molisch H (1897) Untersuchungen uber das Erfrieren der Pflanzen. Fischer, Jena.
44. Murphy C, Wilson JM (1981) Ultrastructural features of chlling-injury in Episcia reptans. Plant Cell Environ 4: 261-265.
45. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K (2006) Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics 6: 212-234.
46. Piqueras A, Olmos E, Hellin E (1994) Cytological changes related with salt tolerance in embryogenic callus of Citrus limon. Plant Cell Tiss Organ Cult 39: 13-18.
47. Ristic Z, Ashworth EN (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation. Protoplasma 172: 111-123.
48. Rosenbaum RM, Wittner M, Lenger M (1969) Mitochondrial and other ultrastructural changes in great alveolar cells of oxygen-adapted and poisoned rats. Lab Invest 20: 516-528.
49. Sam O, Ramirez C, Coronado MJ, Testillano PS, Risueno MC (2003) Changes in tomato leaves induced by NaCl stress: leaf organization and cell ultrastructure. Biol Plant 47: 361-366.
50. Scott I, Logan DC (2008) Mitochondrial morphology transition is an early indicator of subsequent cell death in Arabidopsis. New Phytol 177: 90-101.
51. Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low-temperature response in plants. Bioessays 27: 1048-1059.
52. Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59: 533-551.
53. Skinner JS, Szucs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112: 832-842.
54. Somersalo S, Krause GH (1989) Photoinhibition at chilling temperature. Fluoresence characteristics of unhardened and cold-acclimated spinach leaves. Planta 177: 409-416.
55. Stefanowska M, Kuras M, Kacperska A (2002) Low temperature-induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves. Ann Bot 90: 637-645.
56. Stephens RJ, Bils RF (1965) An atypical mitochondrial form in normal rat liver. J Cell Biol 24: 500-504.
57. Strand A, Hurry V, Gustafsson P, Gardestrom P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12: 605-614.
58. Taylor AO, Craig AS (1971) Plants under climatic stress: I. low temperature, high light effects on chloroplast ultrastructure. Plant Physiol 47: 713-718.
59. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118: 1-8.
60. Thomashow MF (2001) So what's new in the field of plant cold acclimation? Lots! Plant Physiol 125: 89-93.
61. Uemura M, Steponkus PL (1989) Effect of cold acclimation on the incidence of two forms of freezing injury in protoplasts isolated from rye leaves. Plant Physiol 91: 1131-1137.
62. Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 109: 15-30.
63. van Gestel K, Verbelen JP (2002) Giant mitochondria are a response to low oxygen pressure in cells of tobacco (Nicotiana tabacum L.). J Exp Bot 53: 1215-1218.
64. Wise RR, McWilliam J, Naylor AW (1983) A comparative study of low-temperature-induced ultrastructural alterations of three species with differing chilling sensitivities. Plant Cell Environ 6: 525-535.
65. Wright M, Simon EW (1973) Chilling injury in cucumber leaves. J Exp Bot 24: 400-411.
66. Yamazaki T, Kawamura Y, Uemura M (2008) Cryobehavior of the plasma membrane in protoplasts isolated from cold-acclimated Arabidopsis leaves is related to surface area regulation. Plant Cell Physiol 49: 944-957.
67. Yan XX (1995) NaCl-induced amoeboid plastids and mitochondria in meristematic cells of barley. Biol Plant 37: 363-369.
68. Yoshida S, Matsuura-Endo C (1991) Comparison of temperature dependency of tonoplast proton translocation between plants sensitive and insensitive to chilling. Plant Physiol 95: 504-508.
69. Yoshida S, Matsuura C, Etani S (1989) Impairment of tonoplast H-ATPase as an initial physiological response of cells to chilling in mung bean (Vigna radiata [L.] Wilczek). Plant Physiol 89: 634-642.
70. Zhu J, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10: 290-295.