Abstract
Three Coffea species (C. arabica cv. Icatu, C. canephora cv. Apoatã and C. dewevrei) were tested in order to identify and study the mechanisms of tolerance to low, non-freezing
temperatures. Several photosynthesis-related parameters were monitored during a 20-day
period of gradual temperature decrease, from 25/20 °C (day/night) down to 15/10 °C,
during chilling treatments (15/4 °C), and upon rewarming (25/20 °C). Differences were
found among species, both during low temperature exposure and during rewarming. In
general, Coffea species showed cold-induced photoinhibition of photosynthesis, which was attributable
to biochemical (in vivo ribulose-1,5-bisphosphate carboxylase/oxygenase activity and carbohydrate synthesis)
and biophysical (antennae functioning, photosystem II efficiency and linear electron
transport) inactivation, rather than to stomatal constraints. The moderately low temperature
of 15/10 °C was enough to cause a negative impact on net photosynthesis (A), mostly due to low (initial) rubisco activity in all species. However, C. arabica cv. Icatu showed a higher tolerance to chilling and recovered quickly and completely
upon rewarming, as assessed from the impacts on the photosynthetic machinery (e.g.
A
max, F
o, F
v/F
m, F
v′/F
m′, q
P, φ
e, rubisco activity) and on carbohydrate metabolism. Such lesser effects are likely
to be related to the strong increases and higher contents of zeaxanthin, lutein and
β-carotene that presumably increased the ability to dissipate excitation energy and
contributed to protect the photosynthetic apparatus. During cold exposure, a significant
reduction of the α/β carotene ratio, which is considered an acclimation feature, was
observed solely in C. arabica cv. Icatu. However, C. canephora cv. Apoatã and, especially, C. dewevrei showed to be highly cold-sensitive. In these latter species, the photoinhibitory
impairments to photosynthesis were stronger, probably due to the lower contents of
protecting pigments during chilling conditions that lead to a higher vulnerability
to excess excitation energy. Moreover, the mesophyll impairments (e.g. A
max, F
v/F
m, φ
e) became significant even at moderately low temperatures of 15/10 °C, and a lower
ability to recover after chilling exposure was observed. The limitation of in vivo rubisco activity and A
max may have been due to substrate limitation, but disturbances in sugar metabolism could
also play an important role in the expression of chilling sensitivity in C. canephora cv. Apoatã and C. dewevrei.
Key words
Coffea sp. - carotenoids - chilling - chlorophyll a fluorescence - gas exchange - photoinhibition - photosynthetic acclimation - rubisco
activity - sugars - thermal dissipation.
References
- 1
Adams III., W. W., Barker D. H..
Seasonal changes in xanthophyll cycle-dependent energy dissipation in Yucca glauca Nuttall.
Plant Cell Environ..
(1998);
21
501-511
- 2
Adams III., W. W., Demmig-Adams B..
The xanthophyll cycle and sustained thermal energy dissipation in Vinca minor and Euonymus kiautschovicus in winter.
Plant Cell Environ..
(1995);
18
117-127
- 3
Adams III., W. W., Demmig-Adams B., Rosenstiel T. N., Brightwell A. K., Ebbert V..
Photosynthesis and photoprotection in overwintering plants.
Plant Biol..
(2002);
4
545-557
- 4
Adams III., W. W., Demmig-Adams B., Rosenstiel T. N., Ebbert V..
Dependence of photosynthesis and energy dissipation activity upon growth form and
light environment during winter.
Photosynthesis Res..
(2001);
67
51-62
- 5
Adams III., W. W., Demmig-Adams B., Verhoeven A. S., Barker D. H..
“Photoinhibition” during winter stress: Involvement of sustained xanthophyll cycle-dependent
energy dissipation.
Aust. J. Plant Physiol..
(1995);
22
261-276
- 6
Allen D. J., Ort R D..
Impacts of chilling temperatures on photosynthesis in warm-climate plants.
Trends in Plant Sci..
(2001);
6
36-42
- 7
Bauer H., Wierer R., Hatheway W. H., Larcher W..
Photosynthesis of Coffea arabica after chilling.
Physiol. Plant.
(1985);
64
449-454
- 8
Bungard R. A., Ruban A. V., Hibberd J. M., Press M. C., Horton P., Scholes J. D..
Unusual carotenoid composition and a new type of xanthophyll cycle in plants.
Proc. Natl. Acad. Sci. USA.
(1999);
96
1135-1139
- 9
Byrd G. T., Ort D. R., Ögren W. L..
The effects of chilling in the light on the ribulose-1,5-bisphosphate carboxylase/oxygenase
activation in tomato (Lycopersicon esculentum Mill.).
Plant Physiol..
(1995);
107
585-591
- 10
Da Matta F., Maestri M., Mosquim P. R., Barros R. S..
Photosynthesis in coffee (Coffea arabica and C. canephora) as affected by winter and summer conditions.
Plant Sci..
(1997);
128
43-50
- 11
De Las Rivas J., Telfer A., Barber J..
Two coupled beta-carotene molecules protect P680 from photodamage in isolated photosystem two reaction centres.
Biochim. Biophys. Acta.
(1993);
1142
155-164
- 12
Demmig-Adams B., Adams III., W. W..
Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field.
Aust. J. Plant Physiol..
(1996);
23
649-659
- 13 FAOSTAT .Agriculture data online. FAO Statistics database. (1989 - 2001)
- 14
Foyer C. H., Lelandais M., Kunert K. J..
Photooxidative stress in plants.
Physiol. Plant.
(1994);
92
696-717
- 15 Geiger D. R., Servaites J. C., Shieh W.-J..
Balance in the source-sink system: a factor in crop productivity. Baker, N. R. and Thomas, H., eds. Crop Photosynthesis: Spatial and Temporal Determinants
, Topics in Photosynthesis, Vol. 12. Amsterdam; Elsevier (1992): 155-176
- 16
Gilmore A. M..
Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant
chloroplasts and leaves.
Physiol. Plant.
(1997);
99
197-209
- 17
Gilmore A. M., Ball M. C..
Protection and storage of chlorophyll in overwintering evergreens.
Proc. Natl. Acad. Sci. USA.
(2000);
97
11098-11101
- 18
Gray R. G., Chauvin L.-P., Sarhan F., Huner N. P. A..
Cold acclimation and freezing tolerance. A complex interaction of light and temperature.
Plant Physiol..
(1997);
114
467-474
- 19
Grub A., Mächler F..
Photosynthesis and light activation of ribulose-1,5-bisphosphate carboxylase in the
presence of starch.
J. Exp. Bot..
(1990);
41
1293-1301
- 20
Haldimann P..
Low growth temperature-induced changes to pigment composition and photosynthesis in
Zea mays genotypes differing in chilling sensitivity.
Plant Cell Environ..
(1998);
21
200-208
- 21 Hällgreen J.-E., Öquist G..
Adaptations to low temperatures. Alscher, R. T. and Cumming, J. R., eds. Stress Responses in Plants: Adaptation and
Acclimation Mechanisms , Plant Biology Series, Vol. 12. New York; Wiley-Liss Inc.
(1990): 265-293
- 22
Havaux M., Niyogi K. K..
The violaxanthin cycle protects plants from photooxidative damage by more than one
mechanism.
Proc. Natl. Acad. Sci. USA.
(1999);
96
8762-8767
- 23 Hurry V., Huner N., Selstam E., Gardeström P., Öquist G..
Photosynthesis at low growth temperatures. Raghavendra, A. S., ed. Photosynthesis. A comprehensive Treatise. Cambridge; University
Press (1998): 238-249
- 24 Krause G. H..
Photoinhibition induced by low temperatures. Baker, N. R. and Bowyer, J. R., eds. Photoinhibition of Photosynthesis - From Molecular
Mechanisms to the Field. Environmental Plant Biology Series, Oxford; Bios Scientific
Publishers (1994): 331-348
- 25
Kratsch H. A., Wise R. R..
The ultrastructure of chilling stress.
Plant Cell Environ..
(2000);
23
337-350
- 26
Külheim C., Ågren J., Jansson S..
Rapid regulation of light harvesting and plant fitness in the field.
Science.
(2002);
297
91-93
- 27 Leegood R. C..
Effects of temperature on photosynthesis and photorespiration. Smirnoff, N., ed. Environment and Plant Metabolism - Flexibility and Acclimation. Oxford;
Bios Scientific Publishers (1995): 45-62
- 28
Li X.-P., Björkman O., Shih C., Grossman A. R., Rosenquist M., Jansson S., Niyogi K. K..
A pigment-binding protein essential for regulation of photosynthetic light harvesting.
Nature.
(2000);
403
391-395
- 29
Lichtenthaler H. K..
Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.
Methods Enzymol..
(1987);
148
350-382
- 30
Logan B. A., Barker D. H., Demmig-Adams B., Adams III., W. W..
Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the
light environment within an Australian rainforest.
Plant Cell Environ..
(1996);
19
1083-1090
- 31
Ma Y.-Z., Holt N. E., Li X.-P., Niyogi K. K., Fleming G. R..
Evidence for direct carotenoid involvement in the regulation of photosynthetic light
harvesting.
Proc. Natl. Acad. Sci. USA.
(2003);
100
4377-4382
- 32
Maxwell K., Johnson N..
Chlorophyll fluorescence - a practical guide.
J. Exp. Bot..
(2000);
51
659-668
- 33
McCready R. M., Hassid W. Z..
The separation of quantitative estimation of amylose and amylopectin in potato starch.
J. Amer. Chem. Soc..
(1943);
65
1154-1157
- 34
Montané M.-H., Kloppstech K..
The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting
of light their primary function?.
Gene.
(2000);
258
1-8
- 35
Morcuende R., Pérez P., Martínez-Carrasco R., Molino I. M., Puente L. S..
Long- and short-term responses of leaf carbohydrate levels and photosynthesis to decreased
sink demand in soybean.
Plant Cell Environ..
(1996);
19
976-982
- 36
Müller P., Li X.-P., Niyogi K. K..
Non-photochemical quenching. A response to excess light energy.
Plant Physiol..
(2001);
155
1558-1566
- 37
Nelson N..
A photometric adaptation of the Somogyi method for the determination of glucose.
J. Biol. Chem..
(1944);
153
375-380
- 38
Niyogi K. K..
Photoprotection revisited: genetic and molecular approaches.
Annu. Rev. Plant Physiol. Plant Mol. Biol..
(1999);
50
333-359
- 39
Norén H., Svensson P., Stegmark R., Funk C., Adamska I., Andersson B..
Expression of the early light-induced protein but not the PsbS protein is influenced
by low temperature and depends on the developmental stage of the plant in field-grown
pea cultivars.
Plant Cell Environ..
(2003);
26
245-253
- 40
Pogson B. J., Niyogi K. K., Björkman O., Dellapenna D..
Altered xanthophyll compositions adversely affected chlorophyll accumulation and nonphotochemical
quenching in Arabidopsis mutants.
Proc. Natl. Acad. Sci. USA.
(1998);
95
13324-13329
- 41
Ramalho J. C., Campos P. S., Quartin V. L., Silva M. J., Nunes M. A..
High irradiance impairments on photosynthetic electron transport, ribulose-1,5-bisphosphate
carboxylase/oxygenase and N assimilation as a function of N availability in Coffea arabica L. plants.
J. Plant Physiol..
(1999);
154
319-326
- 42
Ramalho J. C., Pons T. L., Groeneveld H. W., Nunes M. A..
Photosynthetic responses of Coffea arabica L. leaves to a short-term high light exposure in relation to N availability.
Physiol. Plant.
(1997);
101
229-239
- 43
Ramalho J. C., Pons T. L., Groeneveld H. W., Azinheira H. G., Nunes M. A..
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..
(2000);
27
43-51
- 44
Siefermann-Harms D..
High-performance liquid chromatography of chloroplast pigments. One-step separation
of carotene and xanthophyll isomers, chlorophylls and pheophytins.
J. Chromatography.
(1988);
448
411-416
- 45 Smith A. W..
Introduction. Clarke, R. J. and Macrae, R., eds. Coffee, Vol. 1, Chemistry. London; Elsevier Applied
Science (1989): 1-41
- 46
Somogyi M..
Notes on sugar determination.
J. Biol. Chem..
(1952);
195
19-23
- 47
Strand Å Hurry V., Henkes S., Huner N., Gustafsson P., Gardeström P., Stitt M..
Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies
increased activities of enzymes in the Calvin cycle and in sucrose-biosynthesis pathway.
Plant Physiol..
(1999);
119
1387-1397
- 48
Thiele A., Schirwitz K., Winter K., Krause G. H..
Increased xanthophyll cycle activity and reduced D1 protein inactivation related to
photoinhibition in two plant systems acclimated to excess light.
Plant Sci..
(1996);
115
237-250
- 49 Wrigley G.. Coffee. Tropical Agriculture Series. Harlow; Longman Scientific and
Technical (1988)
J. C. Ramalho
Centro de Investigação das Ferrugens do Cafeeiro
Inst. Inv. Científica Tropical
Av. República
2784-505 Oeiras
Portugal
Email: cochichor@mail.telepac.pt
Section Editor: B. Demmig-Adams