Chloroplasts of cold-tolerant plants
DOI:
https://doi.org/10.14719/pst.2019.6.4.584Keywords:
Cold-tolerant plants, chloroplast, ultrastructure, stromule, photosynthesisAbstract
Cold is one of the main stress factors affecting plant growth and development. The structure and function of chloroplasts is most vulnerable to cold. This brief review summarizes the influence of low temperature on both chloroplasts’ structure and functioning across cold-tolerant plant species. One of the features of the chloroplast structure is the presence of stromules. We attempted to define a core set of such changes for plants with different habitats. Some changes might be consistent across all species, which were studied; however, some other characteristics were species- or family-specific. Elucidating the interrelation between the mechanisms controlling photosynthesis during cold stress will facilitate the development of strategies to enhance plant tolerance to low-temperature environmental conditions.
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References
1. Information server of Ukrainian Hydrometeorological Center. https://meteo.ua/archive
2. Chen LJ, Xiang HZ, Miao Y, Zhang L, Guo ZF, Zhao XH, Lin JW, Li TL. An overview of cold resistance in plants. - J. Agron. Crop Sci. 2014;200:237-45. https://doi.org/10.1111/jac.12082
3. Kratsch HA, Wise RR. The ultrastructure of chilling stress. Plant Cell Environ. 2000;23(4):337-50. https://doi.org/10.1046/j.1365-3040.2000.00560.x
4. Lütz C, Bergweiler P, Di Piazza L, Holzinger A. Cell organelle structure and function in Alpine and Polar plants are influenced by growth conditions and climate. In Plants in Alpine Regions: Cell Physiology of Adaption and Survival Strategies 2012:43-60. https://doi.org/10.1007/978-3-7091-0136-0_5
5. Meltofte H. Arctic Biodiversity Assessment. Status and Trends in Arctic Biodiversity. Conservation of Arctic Flora and Fauna, Akureyri, Iceland; 2013. https://portals.iucn.org/library/sites/library/files/documents/Bios-Eco-Ter-Pol-027.pdf
6. Smith RL. The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ, editors. Antarctic Biology in a Global Context. Leiden: Backhuys; 2003. p. 234-39.
7. Cavieres LA, Hernández-Fuentes C, Sierra-Almeida A, Kikvidze Z. Facilitation among plants as an insurance policy for diversity in Alpine communities. Funct Ecol. 2016;30(1):52-59. https://doi.org/10.1111/1365-2435.12545
8. Gie?wanowska I, Pastorczyk M, Kellmann-Sopy?a W, Gorniak D, Gorecki R. Morphological and Ultrastructural Changes of Organelles in Leaf Mesophyll Cells of the Arctic and Antarctic Plants of Poaceae Family Under Cold Influence. Arctic Antarct Alp Res. 2015;47(1):17-25. http://dx.doi.org/10.1657/AAAR0014-019
9. Gie?wanowska I, Szczuka E, Bednara J, Górecki R. Anatomical features and ultrastructure of Deschampsia antarctica (Poaceae) leaves from different growing habitats. Ann Bot. 2005, Nov 1; 96(6):1109-19. https://doi.org/10.1093/aob/mci262
10. Gie?wanowska I, Pastorczyk M, Lisowska M, W?grzyn M, Górecki R. Cold stress effects on organelle ultrastructure in polar Caryophyllaceae species. Polish Polar Research, 2014;35(4):627-46. https://doi.org/10.2478/popore-2014-0029
11. Buchner O, Holzinger A, Luetz C. Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ. 2007; 30(11):1347-56. https://doi.org/10.1111/j.1365-3040.2007.01707.x
12. Lütz C, Engel L. Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate? Protoplasma, 2007;231(3-4):183-92. https://doi.org/10.1007/s00709-007-0249-8
13. Fediuk OM, Bilyavska NO, Zolotareva ??. Ultrastructural peculiarities and state of the photosynthetic apparatus in leaves of Galanthus nivalis (Amaryllidaceae) in its spring stage of ontogenesis. Ukrainian Botanical Journal 2017; 74:475-87. https://doi.org/10.15407/ukrbotj74.05.475
14. Szczepanik J, Sowinski P. The occurrence of chloroplast peripheral reticulum in grasses: a matter of phylogeny or a matter of function? Acta Physiol Plant. 2014;36:1133-42 https://doi.org/10.1007/s11738-014-1488-x
15. Newell CA, Natesan SK, Sullivan JA, Jouhet J, Kavanagh TA, Gray JC. Exclusion of plastid nucleoids and ribosomes from stromules in tobacco and Arabidopsis. Plant J. 2012;69:399-410. https://doi.org/10.1111/j.1365-313X.2011.04798.x
16. Schattat MH, Barton KA, Mathur J. The myth of interconnected plastids and related phenomena. Protoplasma 2015; 252(1):359-71. https://doi.org/10.1007/s00709-014-0666-4
17. Schattat M, Griffiths S, Mathur N, Barton K, Wozny M, Dunn N. Differential coloring reveals that plastids do not form networks for exchanging macromolecules. Plant Cell 2012;24:1465-77. https://doi.org/10.1105/tpc.111.095398
18. Schattat M, Klösgen RB, Mathur J. New insights on stromules: stroma filled tubules extended by independent plastids. Plant Signal. 2012;7:1132-37. https://doi.org/10.4161/psb.21342
19. Hanson MR, Hines KM. Stromules: Probing formation and function. Plant Physiol. 2018;176:128-37. https://doi.org/10.1104/pp.17.01287
20. Huner NPA, Öquist G, Sarhan F. Energy balance and acclimation to light and cold. Trends Plant Sci. 1998; 3:224-30. https://doi.org/10.1016/S1360-1385(98)01248-5
21. Pérez-Torres E, Bravo LA, Corcuera LJ, Johnson GN. Is electron transport to oxygen an important mechanism in photoprotection? Contrasting responses from Antarctic vascular plants. Physiol Plant. 2007;130:185-94. https://doi.org/10.1111/j.1399-3054.2007.00899.x
22. Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AL. Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot. 2007;58:3581-90. https://doi.org/10.1093/jxb/erm206
23. Bascuñan-Godoy L, García-Plazaola J, Bravo LA, Corcuera LJ. Leaf functional and micro-morphological photoprotective attributes in two ecotypes of Colobanthus quitensis from the Andes and Maritime Antarctic. Polar Biol. 2010;33:885-96. https://doi.org/10.1007/s00300-010-0765-4
24. Bascuñan-Godoy L, Sanhueza C, Cuba-Díaz M, Zúñiga GE, Corcuera LA, Bravo LA. Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis (Kunt) Bartl. (Caryophyllaceae). BMC Plant Biol. 2012;12:114:1-14. https://doi.org/10.1186/1471-2229-12-114
25. Pérez-Torres E, García A, Dinamarca J, Alberdi M, Gutiérrez A, Gidekel M, et al. The role of photochemical quenching and antioxidants in photoprotection of Deschampsia antarctica. Funct Plant Biol. 2004;31:731-41. https://doi.org/10.1071/FP03082
26. Pérez-Torres E, Bascuñan L, Sierra A, Bravo LA, Corcuera LJ. Robustness of activity of Calvin cycle enzymes after high light and low temperature conditions in Antarctic vascular plants. Pol Biol. 2006;29:909-16. https://doi.org/10.1007/s00300-006-0131-8
27. Zúñiga GE, Alberdi M, Fernández J, Montiel P, Corcuera LJ. Lipid content in leaves of Deschampsia antarctica from the Maritime Antarctic. Phytochemistry, 1994;37:669-72. https://doi.org/10.1016/S0031-9422(00)90335-2
28. Bravo LA, Griffith M. Characterization of antifreeze activity in Antarctic plants. J Exp Bot. 2005;56:1089-96. https://doi.org/10.1093/jxb/eri112
29. Olave-Concha N, Bravo LA, Ruiz-Lara S, Corcuera LJ. Differential accumulation of dehydrin-like proteins by abiotic stresses in Deschampsia antarctica Desv. Pol Biol 2005;28:506-13. https://doi.org/10.1007/s00300-005-0718-5
30. Zúñiga-Feest A, Inostroza P, Vega M, Bravo LA, Corcuera LJ. Sugars and enzyme activity and sugars in the grass Deschampsia antarctica. Antarct. Sci. 2003;15:483-91. https://doi.org/10.1017/S0954102003001597
31. Zúñiga-Feest A, Bascuñan L, Reyes-Diaz M, Bravo LA, Corcuera LJ. Is survival after ice encasement related with organ sugar distribution in the Antarctic plants Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae)? Polar Biol. 2009;32:583-91. https://doi.org/10.1007/s00300-008-0553-6
32. Piotrowicz-Cie?lak AI, Gielwanowska I, Bochenek A, Loro P, Górecki RJ Carbohydrates in Colobanthus quitensis and Deschampsia antarctica. Acta Soc Bot Pol. 2005;74:209-17. https://doi.org/10.5586/asbp.2005.027
33. Fediuk OM, Bilyavska NO, Zolotareva ?? Effects of sucrose on structure and functioning of photosynthetic apparatus of Galanthus nivalis L. leaves exposed to chilling stress. Annals of the Romanian Society for Cell Biology. 2017;21:43–51. https://doi: ?0.ANN/RSCB-2018-0002:RSCB
34. Pérez-Torres E, Dinamarca J, Bravo LA, Corcuera LJ. Responses of Colobanthus quitensis (Kunth) Bartl. to high light and low temperature. Pol Biol. 2004;27:183-89. https://doi.org/10.1007/s00300-003-0577-x
2. Chen LJ, Xiang HZ, Miao Y, Zhang L, Guo ZF, Zhao XH, Lin JW, Li TL. An overview of cold resistance in plants. - J. Agron. Crop Sci. 2014;200:237-45. https://doi.org/10.1111/jac.12082
3. Kratsch HA, Wise RR. The ultrastructure of chilling stress. Plant Cell Environ. 2000;23(4):337-50. https://doi.org/10.1046/j.1365-3040.2000.00560.x
4. Lütz C, Bergweiler P, Di Piazza L, Holzinger A. Cell organelle structure and function in Alpine and Polar plants are influenced by growth conditions and climate. In Plants in Alpine Regions: Cell Physiology of Adaption and Survival Strategies 2012:43-60. https://doi.org/10.1007/978-3-7091-0136-0_5
5. Meltofte H. Arctic Biodiversity Assessment. Status and Trends in Arctic Biodiversity. Conservation of Arctic Flora and Fauna, Akureyri, Iceland; 2013. https://portals.iucn.org/library/sites/library/files/documents/Bios-Eco-Ter-Pol-027.pdf
6. Smith RL. The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ, editors. Antarctic Biology in a Global Context. Leiden: Backhuys; 2003. p. 234-39.
7. Cavieres LA, Hernández-Fuentes C, Sierra-Almeida A, Kikvidze Z. Facilitation among plants as an insurance policy for diversity in Alpine communities. Funct Ecol. 2016;30(1):52-59. https://doi.org/10.1111/1365-2435.12545
8. Gie?wanowska I, Pastorczyk M, Kellmann-Sopy?a W, Gorniak D, Gorecki R. Morphological and Ultrastructural Changes of Organelles in Leaf Mesophyll Cells of the Arctic and Antarctic Plants of Poaceae Family Under Cold Influence. Arctic Antarct Alp Res. 2015;47(1):17-25. http://dx.doi.org/10.1657/AAAR0014-019
9. Gie?wanowska I, Szczuka E, Bednara J, Górecki R. Anatomical features and ultrastructure of Deschampsia antarctica (Poaceae) leaves from different growing habitats. Ann Bot. 2005, Nov 1; 96(6):1109-19. https://doi.org/10.1093/aob/mci262
10. Gie?wanowska I, Pastorczyk M, Lisowska M, W?grzyn M, Górecki R. Cold stress effects on organelle ultrastructure in polar Caryophyllaceae species. Polish Polar Research, 2014;35(4):627-46. https://doi.org/10.2478/popore-2014-0029
11. Buchner O, Holzinger A, Luetz C. Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ. 2007; 30(11):1347-56. https://doi.org/10.1111/j.1365-3040.2007.01707.x
12. Lütz C, Engel L. Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate? Protoplasma, 2007;231(3-4):183-92. https://doi.org/10.1007/s00709-007-0249-8
13. Fediuk OM, Bilyavska NO, Zolotareva ??. Ultrastructural peculiarities and state of the photosynthetic apparatus in leaves of Galanthus nivalis (Amaryllidaceae) in its spring stage of ontogenesis. Ukrainian Botanical Journal 2017; 74:475-87. https://doi.org/10.15407/ukrbotj74.05.475
14. Szczepanik J, Sowinski P. The occurrence of chloroplast peripheral reticulum in grasses: a matter of phylogeny or a matter of function? Acta Physiol Plant. 2014;36:1133-42 https://doi.org/10.1007/s11738-014-1488-x
15. Newell CA, Natesan SK, Sullivan JA, Jouhet J, Kavanagh TA, Gray JC. Exclusion of plastid nucleoids and ribosomes from stromules in tobacco and Arabidopsis. Plant J. 2012;69:399-410. https://doi.org/10.1111/j.1365-313X.2011.04798.x
16. Schattat MH, Barton KA, Mathur J. The myth of interconnected plastids and related phenomena. Protoplasma 2015; 252(1):359-71. https://doi.org/10.1007/s00709-014-0666-4
17. Schattat M, Griffiths S, Mathur N, Barton K, Wozny M, Dunn N. Differential coloring reveals that plastids do not form networks for exchanging macromolecules. Plant Cell 2012;24:1465-77. https://doi.org/10.1105/tpc.111.095398
18. Schattat M, Klösgen RB, Mathur J. New insights on stromules: stroma filled tubules extended by independent plastids. Plant Signal. 2012;7:1132-37. https://doi.org/10.4161/psb.21342
19. Hanson MR, Hines KM. Stromules: Probing formation and function. Plant Physiol. 2018;176:128-37. https://doi.org/10.1104/pp.17.01287
20. Huner NPA, Öquist G, Sarhan F. Energy balance and acclimation to light and cold. Trends Plant Sci. 1998; 3:224-30. https://doi.org/10.1016/S1360-1385(98)01248-5
21. Pérez-Torres E, Bravo LA, Corcuera LJ, Johnson GN. Is electron transport to oxygen an important mechanism in photoprotection? Contrasting responses from Antarctic vascular plants. Physiol Plant. 2007;130:185-94. https://doi.org/10.1111/j.1399-3054.2007.00899.x
22. Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AL. Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot. 2007;58:3581-90. https://doi.org/10.1093/jxb/erm206
23. Bascuñan-Godoy L, García-Plazaola J, Bravo LA, Corcuera LJ. Leaf functional and micro-morphological photoprotective attributes in two ecotypes of Colobanthus quitensis from the Andes and Maritime Antarctic. Polar Biol. 2010;33:885-96. https://doi.org/10.1007/s00300-010-0765-4
24. Bascuñan-Godoy L, Sanhueza C, Cuba-Díaz M, Zúñiga GE, Corcuera LA, Bravo LA. Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis (Kunt) Bartl. (Caryophyllaceae). BMC Plant Biol. 2012;12:114:1-14. https://doi.org/10.1186/1471-2229-12-114
25. Pérez-Torres E, García A, Dinamarca J, Alberdi M, Gutiérrez A, Gidekel M, et al. The role of photochemical quenching and antioxidants in photoprotection of Deschampsia antarctica. Funct Plant Biol. 2004;31:731-41. https://doi.org/10.1071/FP03082
26. Pérez-Torres E, Bascuñan L, Sierra A, Bravo LA, Corcuera LJ. Robustness of activity of Calvin cycle enzymes after high light and low temperature conditions in Antarctic vascular plants. Pol Biol. 2006;29:909-16. https://doi.org/10.1007/s00300-006-0131-8
27. Zúñiga GE, Alberdi M, Fernández J, Montiel P, Corcuera LJ. Lipid content in leaves of Deschampsia antarctica from the Maritime Antarctic. Phytochemistry, 1994;37:669-72. https://doi.org/10.1016/S0031-9422(00)90335-2
28. Bravo LA, Griffith M. Characterization of antifreeze activity in Antarctic plants. J Exp Bot. 2005;56:1089-96. https://doi.org/10.1093/jxb/eri112
29. Olave-Concha N, Bravo LA, Ruiz-Lara S, Corcuera LJ. Differential accumulation of dehydrin-like proteins by abiotic stresses in Deschampsia antarctica Desv. Pol Biol 2005;28:506-13. https://doi.org/10.1007/s00300-005-0718-5
30. Zúñiga-Feest A, Inostroza P, Vega M, Bravo LA, Corcuera LJ. Sugars and enzyme activity and sugars in the grass Deschampsia antarctica. Antarct. Sci. 2003;15:483-91. https://doi.org/10.1017/S0954102003001597
31. Zúñiga-Feest A, Bascuñan L, Reyes-Diaz M, Bravo LA, Corcuera LJ. Is survival after ice encasement related with organ sugar distribution in the Antarctic plants Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae)? Polar Biol. 2009;32:583-91. https://doi.org/10.1007/s00300-008-0553-6
32. Piotrowicz-Cie?lak AI, Gielwanowska I, Bochenek A, Loro P, Górecki RJ Carbohydrates in Colobanthus quitensis and Deschampsia antarctica. Acta Soc Bot Pol. 2005;74:209-17. https://doi.org/10.5586/asbp.2005.027
33. Fediuk OM, Bilyavska NO, Zolotareva ?? Effects of sucrose on structure and functioning of photosynthetic apparatus of Galanthus nivalis L. leaves exposed to chilling stress. Annals of the Romanian Society for Cell Biology. 2017;21:43–51. https://doi: ?0.ANN/RSCB-2018-0002:RSCB
34. Pérez-Torres E, Dinamarca J, Bravo LA, Corcuera LJ. Responses of Colobanthus quitensis (Kunth) Bartl. to high light and low temperature. Pol Biol. 2004;27:183-89. https://doi.org/10.1007/s00300-003-0577-x
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01-10-2019
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Bilyavska NO, Fediuk OM, Zolotareva EK. Chloroplasts of cold-tolerant plants. Plant Sci. Today [Internet]. 2019 Oct. 1 [cited 2024 May 9];6(4):407-11. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/584
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