Abstract
Climate changes implicate an increase in climate instability and the occurrence of extreme temperature in the environment. In this context, the differential triggering of cold tolerance mechanisms among coffee plants, highlighting the existence of important genetic variability, is of up most importance to be exploited in genotype screening and breeding programs. This review deals with the identification and triggering of acclimation mechanisms that shield key functions and structures of photosynthesis, with a particular emphasis on experiments under environmental controlled conditions. These mechanisms allow plants to perform metabolic and structural adjustments, particularly under conditions of a gradual cold exposure, simulating the effects happening in the field under cold periods. Detailed attention is given to the strengthening of the antioxidative system and to the dynamics of the lipid matrix components in chloroplast membranes, since they were found to constitute crucial traits to an effective long-term acclimation and, therefore, to guarantee the economic sustainability of this important tropical cash crop, particularly in cultivation areas prone to the occurrence of low positive temperatures.
Similar content being viewed by others
Abbreviations
- Amax :
-
Photosynthetic capacity
- APX:
-
Ascorbate peroxidase
- C16:0:
-
Palmitic acid
- C16:1t :
-
3-trans-Hexadecenoic acid
- C18:0:
-
Stearic acid
- C18:1:
-
Oleic acid
- C18:2:
-
Linoleic acid
- C18:3:
-
Linolenic acid
- Chl:
-
Chlorophyll
- 3Chl*:
-
Triplet state of Chl
- CGA:
-
Chlorogenic acid
- CQA:
-
Caffeoylquinic acid
- Ci :
-
Internal CO2 concentration
- Cu/Zn–SOD:
-
Cu/Zn–superoxide dismutase
- Cyt:
-
Cytochrome
- DBI:
-
Double bond index
- DGDG:
-
Digalactosyldiacylglycerol
- DHAR:
-
Dehydroascorbate reductase
- FA:
-
Fatty acid
- ϕe :
-
Estimate of the quantum yield of photosynthetic non-cyclic electron transport
- Fv/Fm :
-
Maximal photochemical efficiency of PS II
- Fv′/Fm′:
-
Photochemical efficiency of PS II under photosynthetic steady-state conditions
- GL:
-
Galactolipid
- GRed:
-
Glutathione reductase
- gs :
-
Stomatal conductance to water vapour
- H2O2 :
-
Hydrogen peroxide
- LHCP:
-
Light harvesting complex proteins
- MDH:
-
Malate dehydrogenase
- MDHAR:
-
Monodehydroascorbate reductase
- MGDG:
-
Monogalactosyldiacylglycerol
- NPQ:
-
Non-photochemical quenching
- 1O2 :
-
Singlet oxygen
- O •−2 :
-
Superoxide anion radical
- •OH:
-
Hydroxyl radical
- qP :
-
Photochemical quenching
- PA:
-
Phosphatidic acid
- PC:
-
Phosphatidylcholine
- PG:
-
Phosphatidylglycerol
- PK:
-
Pyruvate kinase
- PI:
-
Phosphatidylinositol
- PL:
-
Phospholipid
- Pn :
-
Net photosynthetic rate
- PQ:
-
Plastoquinone
- PSI and II:
-
Photosystems I and II
- ROS:
-
Reactive oxygen species
- RuBisCo:
-
Ribulose-1,5-bisphosphate carboxylase/oxygenase
- TFA:
-
Total fatty acids
References
Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42
Alonso A, Queiroz CS, Magalhães AC (1997) Chilling stress leads to increased cell membrane rigidity in roots of coffee (Coffea arabica L.) seedlings. Biochim Biophys Acta 1323:75–84
Amaral JAT, DaMatta FM, Rena AB (2001) Effects of fruiting on the growth of Arabica coffee trees as related to carbohydrate and nitrogen status and to nitrate reductase activity. Braz J Plant Physiol 13:66–74
Amaral JAT, Rena AB, Amaral JFT (2006) Crescimento vegetativo sazonal do cafeeiro e sua relação com fotoperíodo, frutificação, resistência estomática e fotossíntese. Pesquisa Agropecuária Brasileira 41:377–384
Aphalo PJ, Lahti M, Lehto T, Repo T, Rummukainen A, Mannerkoski H, Finér L (2006) Responses of silver birch saplings to low soil temperature. Silva Fennica 40:429–442
Aroca R, Vernieri P, Irigoyen JJ, Sánchez-Díaz 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
Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS Scientific Publishers Ltd., Oxford, pp 129–142
Assad ED, Pinto HS, Zullo J Jr, Ávila AMH (2004) Impacto das mudanças climáticas no zoneamento agroclimático do café no Brasil. Pesquisa Agropecuária Brasileira 39:1057–1064
Barros RS, Maestri M (1974) Influência dos fatores climáticos sobre a periodicidade de crescimento vegetativo do café (Coffea arabica L.). Revista Ceres 21:268–279
Barros RS, Mota JW, DaMatta FM, Maestri M (1997) Decline of vegetative growth in Coffea arabica L. in relation to leaf temperature, water potential and stomatal conductance. Field Crops Res 54:65–72
Batista-Santos P, Lidon FC, Fortunato A, Leitão AE, Lopes E, Partelli F, Ribeiro AI, Ramalho JC (2011) The impact of cold on photosynthesis in genotypes of Coffea spp.—photosystem sensitivity, photoprotective mechanisms and gene expression. J Plant Physiol 168:792–806
Bauer H, Wierer R, Hatheway WH, Larcher W (1985) Photosynthesis of Coffea arabica after chilling. Physiol Plant 64:449–454
Bauer H, Comploj A, Bodner M (1990) Susceptibility to chilling of some Central-African cultivars of Coffea arabica. Field Crops Res 24:119–129
Bicho NC, Oliveira JFS, Lidon FC, Ramalho JC, Leitão AE (2011) O café: origens, produção, processamento e definição de qualidade. Escolar Editora, Lisbon, p 171. ISBN 978-972-592-322-1
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
Camargo AP (1985) O clima e a cafeicultura no Brasil. Informe Agropecuário, Belo Horizonte 11(126):13–26
Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292
Cavatte PC, Oliveira AAG, Morais LE, Martins SCV, Sanglard LMVP, DaMatta FM (2012) Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis. Physiol Plant 114:111–122
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought: from genes to the whole plant. Funct Plant Biol 30:239–264
Coste R (1992) Coffee: the plant and the product. MacMillan, London, p 328
DaMatta FM (2004) Ecophysiological constraints on the production of shaded and unshaded coffee: a review. Field Crops Res 86:99–114
DaMatta FM, Ramalho JC (2006) Impacts of drought and temperature stress on coffee physiology and production: a review. Braz J Plant Physiol 18:55–81
DaMatta FM, Maestri M, Mosquim PR, Barros RS (1997) Photosynthesis in coffee (Coffea arabica and C. canephora) as affected by winter and summer conditions. Plant Sci 128:43–50
Davis AP, Govaerts R, Bridson DM, Stoffelen P (2006) An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Bot J Linn Soc 152:465–512
Davis AP, Gole TW, Baena S, Moat J (2012) The impact of climate change on indigenous arabica coffee (Coffea arabica): predicting future trends and identifying priorities. PLoS ONE 7(11):e47981
Dias AS, Barreiro MG, Campos PS, Ramalho JC, Lidon FC (2010) Wheat celular thermotolerance under heat stress. J Agron Crop Sci 196(2):100–108
Dong JZ, Dunstan DI (1997) Endochitinase and -1,3-glucanase genes are developmentally regulated during somatic embryogenesis in Picea glauca. Planta 201:189–194
Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44
Fortunato A, Lidon FC, Batista-Santos P, Leitão AE, Pais IP, Ribeiro AI, Ramalho JC (2010) Biochemical and molecular characterization of the antioxidative system of Coffea sp. under cold conditions in genotypes with contrasting tolerance. J Plant Physiol 167:333–342
Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717
Gao J–J, Li T, Yu X-C (2009) Gene expression and activities of SOD in cucumber seedlings were related with concentrations of Mn2+, Cu2+, or Zn2+ under low temperature stress. Agric Sci China 8:678–684
Gay C, Estrada F, Conde C, Eakin H, Villers L (2006) Potential impacts of climate change on agriculture: a case of study of coffee production in Veracruz, Mexico. Clim Change 79:259–288
Gombos Z, Murata N (1998) Genetic engineering of the unsaturation of membrane glycerolipid: effects on the ability of the photosynthetic machinery to tolerate temperature stress. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics, series advances in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 249–262
Gorsuch PA, Pandey S, Atkin OK (2010) Thermal de-acclimation: how permanent are leaf phenotypes when cold-acclimated plants experience warming? Plant Cell Environ 33:1124–1137
Goulao LF, Fortunato AS, Ramalho JC (2012) Selection of reference genes for normalizing quantitative real-time PCR gene expression data with multiple variables in Coffea spp. Plant Mol Biol Rep 30:741–759
Grace SC (2005) Phenolics as antioxidants. In: Smirnoff N (ed) Antioxidants and reactive oxygen in plants. Blackwell, Oxford, pp 141–168
Gray GR, Ivanov AG, Krol M, Williams JP, Kahn MU, Myscich EG, Huner NPA (2005) Temperature and light modulate the trans-Δ3-hexadecenoic acid content of phosphatidylglycerol: light-harvesting complex II organization and non-photochemical quenching. Plant Cell Physiol 46:1272–1282
Harwood JL (1997) Plant lipid metabolism. In: Dey PM, Harborne JB (eds) Plant biochemistry. Academic Press, San Diego, pp 237–271
Harwood JL (1998) Involvement of chloroplast lipids in the reaction of plants submitted to stress. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Series advances in photosynthesis, vol 6. Kluwer Academic Publishers, Dordrecht, pp 287–302
Hideg E, Kós PB, Vass I (2007) Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol Plant 131:33–40
Iba I (2002) Acclimation response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245
International Coffee Organization (ICO) (2013) Statistics. Disponível em. http://www.ico.org/trade_statistics.asp. Accessed 7 Oct 2013
Kodama H, Horiguchi G, Nishiuchi T, Nishimura M, Iba K (1995) Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves. Plant Physiol 107:1177–1185
Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350
Larcher W (1981) Effects of low temperature stress and frost injury on plant productivity. In: Johnson CB (ed) Physiological processes limiting plant productivity. Butterworths, London, pp 253–269
Leshem Y (1992) Plant membranes: a biophysical approach to structure, development and senescence. Kluwer Academic Publishers, Dordrecht
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Libardi VCM, Amaral JAT, Amaral JFT (1998) Crescimento vegetativo sazonal do cafeeiro (Coffea canephora Pierre var. Conilon) no sul do Estado do Espírito Santo. Revista Brasileira de Agrometeorologia 6:23–28
Lidon FC, Henriques FS (1993) Oxygen-metabolism in higher plant chloroplasts. Photosynthetica 29(2):249–279
Lidon FC, Loureiro AS, Vieira DE, Bilho EA, Nobre P, Costa R (2001a) Photoinhibition in chilling stressed wheat and maize. Photosynthetica 39(2):161–166
Lidon FC, Ribeiro G, Santana H, Marques H, Correia K, Gouveia S (2001b) Photoinhibition in chilling stressed Leguminosae: comparison of Vicia fava and Pisum sativum. Photosynthetica 39(1):17–22
Lima ALS, DaMatta FM, Pinheiro AH, Totola MR, Loureiro ME (2002) Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. Environ Exp Bot 47:239–247
Logan BA (2005) Reactive oxygen species and photosynthesis. In: Smirnoff N (ed) Antioxidants and reactive oxygen in plants. Blackwell, Oxford, pp 250–267
Ma Y-Z, Holt NE, Li X-P, Niyogi KK, Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100:4377–4382
Marraccini P, Freire LP, Alves GSC, Vieira NG, Vinecky F, Elbelt S, Ramos HJO, Montagnon C, Vieira LGE, Leroy T, Pot D, Silva VA, Rodrigues GC, Andrade AC (2011) RBCS1 expression in coffee: coffea orthologs, Coffea arabica homeologs, and expression variability between genotypes and under drought stress. BMC Plant Biol 11:85
Marraccini P, Vinecky F, Alves GSC, Ramos HJO, Elbelt S, Vieira NG, Carneiro FA, Sujii PS, Alekcevetch JC, Silva VA, DaMatta FM, Ferrão MAG, Leroy T, Pot D, Vieira LGE, Silva FR, Andrade AC (2012) Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora. J Exp Bot 63:4191–4212
Marré WB (2012) Crescimento vegetativo e acúmulo de nutrientes em diferentes genótipos do cafeeiro Conilon. Universidade Federal do Espírito Santo, São Mateus
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London, pp 889. ISBN 0-12-473542-6
Matiello JB (1998) Café Conillon: Como Plantar, Tratar, Colher, Preparar e Vender. MM Produções Gráficas, Rio de Janeiro
Mills RF, Doherty ML, López-Marqués RL, Weimar T, Dupree P, Palmgren MG, Pittman JK, Williams LE (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol 146:116–128
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mondego JM, Vidal RO, Carazzolle MF, Tokuda EK, Parizzi LP, Costa GG, Pereira LF, Andrade AC, Colombo CA, Vieira LGE, Pereira GAG (2011) An EST-based analysis identifies new genes and reveals distinctive gene expression features of Coffea arabica and Coffea canephora. BMC Plant Biol 11:30
Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748
Murata N, Siegenthaler P-A (1998) Lipids in photosynthesis: an overview. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics, series advances in photosynthesis, vol 6. Kluwer Academic Publishers, Dordrecht, pp 1–20
Navari-Izzo F, Ricci F, Vazzana C, Quartacci M (1995) Unusual composition of thylakoid membranes of the resurrection plant Boea hygroscopica: changes in lipids upon dehydration and rehydration. Physiol Plant 94:135–142
Nazareno RB, Oliveira CAS, Sanzonowicz C, Sampaio JBR, Silva JCP, Guerra AF (2003) Crescimento inicial do cafeeiro Rubi em respostas a doses de nitrogênio fósforo e potássio e a regime hídricos. Pesquisa Agropecuária Brasileira 38:903–910
Oliveira JG, Alves PLCA, Magalhães AC (2002) The effect of chilling on the photosynthetic activity in coffee (Coffea arabica L.) seedlings. The proactive action of chloroplastid pigments. Braz J Plant Physiol 14:95–104
Öquist G (1982) Seasonally induced changes in acyl lipids and fatty acids of chloroplast thylakoids of Pinus silvestris. A correlation between the level of unsaturation of monogalatosyldiglyceride and the rate of electron transport. Plant Physiol 69:869–875
Partelli FL, Vieira HD, Viana AP, Batista-Santos P, Leitão AE, Ramalho JC (2009) Low temperature impact on photosynthetic parameters in coffee genotypes. Pesquisa Agropecuária Brasileira 44:1404–1415
Partelli FL, Vieira HD, Silva MG, Ramalho JC (2010) Seasonal vegetative growth of different age branches of Conilon coffee tree. Semina: Ciências Agrárias 31:619–626
Partelli FL, Batista-Santos P, Scotti-Campos P, Pais IP, Quantin VL, Vieira HD, Ramalho JC (2011) Characterization of the main lipid components of chloroplast membranes and cold induced changes in Coffea spp. Environ Exp Bot 74:194–204
Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466
Pinheiro AH, DaMatta FM, Chaves ARM, Fontes EPB, Loureiro ME (2004) Drought tolerance in relation to protection against oxidative stress in clones of Coffea canephora subjected to long-term drought. Plant Sci 167:1307–1314
Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM (2010) Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. J Plant Physiol 167:1052–1060
Praxedes SC, DaMatta FM, Loureiro ME, Ferrão MAG, Cordeiro AT (2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environ Exp Bot 56:263–273
Queiroz CGS, Mares-Guia ML, Magalhães AC (2000) Microcalorimetric evaluation of metabolic heat rates in coffee (Coffea arabica L.) roots of seedlings subjected to chilling stress. Thermochim Acta 351:33–37
Ramalho JC, Pons T, Groeneveld H, Nunes MA (1997) Photosynthetic responses of Coffea arabica L. leaves to a short-term high light exposure in relation to N availability. Physiol Plant 101:229–239
Ramalho JC, Campos PS, Teixeira M, Nunes MA (1998) Nitrogen dependent changes in antioxidant systems and in fatty acid composition of chloroplast membranes from Coffea arabica L. plants submitted to high irradiance. Plant Sci 135:115–124
Ramalho JC, Campos PS, Quartin VL, Silva MJ, Nunes MA (1999) High irradiance impairments on electron transport, ribulose-1,5-bisphosphate carboxylase/oxygenase and N assimilation as function of N availability in Coffea arabica L. plants. J Plant Physiol 154:319–326
Ramalho JC, Pons T, Groeneveld H, Azinheira HG, Nunes MA (2000) Photosynthetic acclimation to high light conditions in mature leaves of Coffea arabica L.: role of xanthophylls, quenching mechanisms and nitrogen nutrition. Aust J Plant Physiol 27:43–51
Ramalho JC, Marques NC, Semedo JN, Matos MC, Quartin VL (2002) Photosynthetic performance and pigment composition of leaves from two tropical species is determined by light quality. Plant Biol 4:112–120
Ramalho JC, Quartin V, Leitão AE, Campos PS, Carelli ML, Fahl JI, Nunes MA (2003) Cold acclimation ability of photosynthesis among species of the tropical Coffea genus. Plant Biol 5:631–641
Ramalho JC, Fortunato AS, Goulao LF, Lidon FC (2013a) Cold-induced changes in mineral content in Coffea spp. leaves: identification of descriptors for tolerance assessment. Biol Plant 57(3):495–506
Ramalho JC, Rodrigues AP, Semedo JN, Pais I, Martins LD, Simões-Costa MC, Leitão AE, Fortunato AS, Batista-Santos P, Palos I, Tomaz MA, Scotti-Campos P, Lidon FC, DaMatta FM (2013b) Sustained photosynthetic performance of Coffea spp. under long-term enhanced [CO2]. PLOS ONE. 8(12):e82712. doi:10.1371/journal.pone.0082712
Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149
Rena AB (2000) Consequências fisiológicas das baixas temperaturas no cafeeiro. Circular Técnica. Lavras: EPAMIG/CRSM, n. 99
Routaboul JM, Fischer S, Browse J (2000) Trienoic fatty acids are required to maintain chloroplast function at low temperature. Plant Physiol 124:1697–1705
Sasaki C, Vårum KM, Itoh Y, Tamoi M, Fukamizo T (2006) Rice chitinases: sugar recognition specificities of the individual subsites. Glycobiology 16:1242–1250
Scotti-Campos P, Pais IP, Partelli FL, Batista-Santos P, Ramalho JC (2014) Phospholipids profile in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability. J Plant Physiol 171:243–249
Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217
Siegenthaler PA, Trémolières A (1998) Role of acyl lipids in the function of photosyntheticmembranes in higher plants. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics, series advances in photosynthesis, vol 6. Kluwer Academic Publishers, Dordrecht, pp 145–173
Silva EA, DaMatta FM, Ducatti C, Regazzi AJ, Barros RS (2004) Seasonal changes in vegetative growth and photosynthesis of Arabica coffee trees. Field Crops Res 89:349–357
Smirnoff N (1995) Metabolic flexibility in relation to environment. In: Smirnoff N (ed) Environment and plant metabolism. Flexibility and acclimation. BIOS Scientific Publishers, Oxford, pp 1–16
Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff N (ed) Antioxidants and reactive oxygen in plants. Blackwell, Oxford, pp 1–24
Strauss AJ, Krüger GHJ, Strasser RJ, Van Heerden PDR (2007) The role of low soil temperature in the inhibition of growth and PSII function during dark chilling in soybean genotypes of contrasting tolerance. Physiol Plant 131:89–105
Torres-Franklin M-L, Gigon A, Melo DF, Zuily-Fodil Y, Pham-Thi A-T (2007) Drought stress and rehydration affect the balance between MGDG and DGDG synthesis in cowpea leaves. Physiol Plant 131:201–210
Uemura M, Joseph RA, Steponkus PL (1995) Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol 109:15–30
Vijayan P, Routaboul J-M, Okada J (1998) A genetic approach to investigating membrane lipid structure and photosynthetic function. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics, series advances in photosynthesis, vol 6. Kluwer Academic Publishers, Dordrecht, pp 263–285
Wada H, Gombos Z, Murata N (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc Natl Acad Sci USA 91:4273–4277
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye J-Y, Mi H (2006a) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol 141:465–474
Wang X, Li W, Li M, Welti R (2006b) Profiling lipid changes in response to low temperatures. Physiol Plant 126:90–96
Webb MS, Green BR (1991) Biochemical and biophysical properties of thylakoid acyl lipids. Biochim Biophys Acta 1060:133–158
Willson KC (1999) Coffee, cocoa and tea. CAB International, Wallingford
Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
Zhu S-Q, Zhao H, Liang J-S, Ji B-H, Jiao D-M (2008) Relationships between phosphatidylglycerol molecular species of thylakoid membrane lipids and sensitivities to chilling-induced photoinhibition in rice. J Integr Plant Biol 50:194–202
Zullo J, Pinto HS, Assad ED, Ávila AMH (2011) Potential for growing Arabica coffee in the extreme south of Brazil in a warmer world. Clim Change 109:535–548
Acknowledgments
The authors thank E. Lopes and I. Palos (IICT) for technical support. This work was supported by Portuguese National Funds of Fundação para a Ciência e a Tecnologia, through the Grant SFRH/BPD/78619/2011 (P. Batista-Santos).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ramalho, J.C., DaMatta, F.M., Rodrigues, A.P. et al. Cold impact and acclimation response of Coffea spp. plants. Theor. Exp. Plant Physiol 26, 5–18 (2014). https://doi.org/10.1007/s40626-014-0001-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-014-0001-7