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Drought tolerance of two field-grown clones of Coffea canephora
Plant Science 164 (2003) 111 /117 www.elsevier.com/locate/plantsci
Drought tolerance of two field-grown clones of Coffea canephora Fa´bio M. DaMatta a,*, Agnaldo R.M. Chaves a, Hugo A. Pinheiro a, Carlos Ducatti b, Marcelo E. Loureiro a b
a Departamento de Biologia Vegetal, Universidade Federal de Vic¸osa, 36571-000 Vic¸osa, MG, Brazil Centro de Iso´topos Esta´veis Ambientais, Departamento de Fı´sica e Biofı´sica, Universidade do Estado de Sa˜o Paulo, 18618-000 Botucatu, SP, Brazil
Received 12 March 2002; received in revised form 2 October 2002; accepted 2 October 2002
Abstract We compared tolerance to soil drought of two field-grown clones of Coffea canephora (clone 46, drought-sensitive; and clone 120, drought-tolerant). Under irrigation, there were no marked differences between the clones in water relation parameters, gas exchange and total leaf area. Under rainfed conditions, clone 46 showed osmotic adjustment and increased tissue rigidity. These adjustments, however, were incapable of preventing substantial decreases in xylem pressure potential. By contrast, clone 120 did not exhibit osmotic adjustment, but was able to increase tissue elasticity and to maintain xylem pressure potentials to a greater extent than clone 46 (despite having twice the total leaf area of this clone). Stomatal conductance was lowered by drought in clone 120 but not in clone 46. Carbon assimilation per unit leaf area in both clones remained unaffected under stress. Long-term water use efficiency (WUE), as estimated through carbon isotope discrimination, was consistently greater in clone 120 than in clone 46. Because of these traits, clone 120 was better able to postpone dehydration and to maintain whole-tree photosynthesis. It is proposed that these features should decisively contribute to buffer its productivity in drought-prone areas. # 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Carbon isotope discrimination; Coffea canephora ; Coffee; Drought stress; Gas exchange; Water relations
1. Introduction The ability of a crop to produce satisfactorily in areas subjected to water deficit has been termed drought tolerance regardless of how the ability develops. The mechanisms of drought tolerance have been categorised by Kramer and Boyer [1] as: (i) drought avoidance; (ii) dehydration tolerance; and (iii) dehydration postponement. Some species can avoid drought by maturing rapidly before the onset of dry conditions or reproducing only after rain. Others allow dehydration of the
Abbreviations: A, net carbon assimilation rate; Ci/Ca, ratio of internal to ambient CO2 concentration; E , transpiration rate; gs, stomatal conductance to water vapour; RWC, relative water content; WUE, water use efficiency; D, carbon isotope discrimination; o , bulk leaf modulus of elasticity; C md, midday xylem pressure potential; C p, turgor potential; C pd, predawn xylem pressure potential; Cx, xylem pressure potential; C p, osmotic potential; Cp(max), osmotic potential at maximum turgor; Cp(0), osmotic potential at zero turgor. * Corresponding author. Fax: /55-31-3899-2580 E-mail address: [email protected] (F.M. DaMatta).
tissues and simply tolerate it by continuing to grow when dehydrated or surviving severe dehydration. Still other species can postpone dehydration by growing deep roots and/or effectively controlling water loss chiefly through stomatal closure and decreased leaf area, thus improving plant water status and turgor maintenance. Osmotic adjustment, defined as a net increased solute concentration, can contribute to turgor maintenance and thereby to turgor-mediated processes such as elongation growth and photosynthesis [2]. Although osmotic adjustment may be perceived as a survival mechanism, it does enable physiological activity to be maintained, albeit at a low level throughout a period of water deficit [3]. Turgor maintenance can also be achieved through increases in tissue elasticity, which may permit attainment of a low water potential without the development of detrimental water deficits. By contrast, decreases in tissue elasticity may allow a lower water potential to be reached for a given change in water volume, thus facilitating continued water uptake from drying soil [1].
0168-9452/02/$ - see front matter # 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 8 - 9 4 5 2 ( 0 2 ) 0 0 3 4 2 - 4
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Water use efficiency (WUE), defined as the ratio of carbon gain to water loss, is thought to play an important role in acclimation, productivity and the probability of survival under drought stress [4,5]. Plants can achieve a high WUE through either a high rate of net carbon assimilation (A ) or a low rate of transpiration (E ), or both. In C3 plants, the stable carbon isotope discrimination (D) is related to whole-plant WUE through, amongst other factors, the stomatal control of gas exchange and the degree of discrimination against 13 C with changing ratio of internal to ambient CO2 concentrations, Ci/Ca [6]. Typically, plants with a favourable water status have a high Ci/Ca and are depleted in 13C, whereas droughted plants have a low Ci/Ca and are enriched in 13C, reflecting the trade-off between A and E . From about 90 species of Coffea , only Coffea arabica (Arabica coffee) and Coffea canephora (Robusta coffee) are significant in the world commercial trade. The volume of business generated from Robusta coffee on the international coffee market has been steadily increasing for half a century, and presently this species accounts for about one-third of the coffee consumed world-wide [7]. Robusta coffee is native to lowland forest of the Congo river basin (Africa) with a typical equatorial climate in which average temperature is between 24 and 26 8C and an abundant rainfall distributed over a 9 /10-month period, and atmospheric humidity at a nearly constant level approaching saturation [8,9]. Under plantation schemes, a necessary minimum annual rainfall of 1250 mm, or even 1550 mm, has been quoted, but this would require an even distribution [8]. In the main Brazilian area producing Robusta coffee (Espı´rito Santo State), there is an increasing trend in expanding cultivation towards marginal and degraded lands where water availability constitutes one of the major problems. In these areas, during the dry season, which lasts from 4 to 7 months, evaporation by far exceeds rainfall and, within the rainy season, rainfall pattern and amount are to a great extent unpredictable. Such conditions could be expected to largely restrict the productive potential of Robusta coffee. Local experience has shown that crop yield under rainfed conditions may decrease by about 40% or even as much as by 80% in dry years. Irrigation has been successfully employed, enabling the plant to be a profitable crop and preventing crop failure in dry years. However, costs involved for purchasing and installing irrigation equipment are rather expensive and immediately pose a problem for the profitability of its use, particularly in small farms where Robusta coffee is mostly cultivated. In addition, a permanent, reliable source of water for irrigation is not always available. Over the last 15 years vegetative methods of selection have improved significantly the clonal performance of
Robusta coffee under drought conditions, rendering coffee cropping less dependent on irrigation. Clones were originally selected from commercial, open-pollinated plantations from Espı´rito Santo State by visual assessment of trees with suspected superior performance under certain climatic conditions. However, performance has been evaluated exclusively in terms of harvestable crop, without examination of how physiological parameters may contribute to drought tolerance in this species [10]. In this work, we have evaluated two highly productive clones when grown under irrigation; under limited soil water, however, both survival and productivity are severely impaired in the droughtsensitive clone, while only marginal effects on productivity have been noted to occur in the drought-tolerant clone [11,12]. A major goal of this study was to physiologically examine how these clones respond to soil drought in order to explain the differences in their yield responses.
2. Material and methods 2.1. General The study site is located in the Experimental Station of Sooretama (19824?S, 40831W, 30 m elevation), Espı´rito Santo State, south-eastern Brazil. The soil at the site is a flat, deep, sandy Oxisol with a volumetric water content 15.7% at field capacity and 8.3% at permanent wilting point; it is extensively found in areas of cultivation of Robusta coffee in that region. The site receives an average annual rainfall of 1200 mm with a marked dry season from March/April to September/ October. Average annual temperature is 23.5 8C. Uniform seedlings of two clones of C. canephora Pierre var. Conillon (clone 46, drought-sensitive; and clone 120, drought-tolerant) with four leaf pairs, obtained as rooted stem cuttings, were planted in two adjacent plots in April 1996 at a spacing of 2.5 m between rows and 1.0 m within rows. During the first 2 years after planting, all trees were irrigated equally to guarantee the uniformity of plant development. Irrigation, applied by overhead sprinklers, was scheduled whenever potential soil water deficit reached 20 mm, as estimated from pan evaporation. The trees were trained with four heads and received routine agricultural practices suitable for commercial bean production including hoeing, fertilisation and chemical control of insect and pathogen attack. After late March 1998, one plot was maintained without any irrigation (rainfed conditions) while the other continued receiving irrigation as outlined above. From April through September 1998 there was no appreciable rainfall. Field measurements were conducted on cloudless days from June 02 to 06, 1998, starting 55 days after last rainfall. Compara-
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tively, clone 46 has larger leaves, shorter internodes, shorter plagiotropic branches and slightly denser crowns than clone 120. No significant difference in plant height was observed between the clones, regardless of the watering regime. Probably, the rainless period was not long enough to lead to reductions in height in rainfed plants. Unless otherwise stated, sampling and measurements were made on six trees randomly chosen per each clone selected within each water regime, using the youngest, fully expanded, upper-canopy, sunlit leaves (one leaf per tree). Measurements of xylem pressure potential (C x) and gas exchange for each tree were repeated once in another day; for data analysis, observations on each day were treated as subsamples. Environmental conditions of humidity, air temperature and solar radiation, as monitored by a meteorological station localised in the Experimental Station, did not differ significantly among the measurement days. Thus, day-to-day variation in those measurements was assumed to reflect differences in both clonal and irrigation treatments. 2.2. Water relations Leaf C x was measured in the field at both predawn (C pd) and midday (C md) using a Scholander-type pressure chamber. The sampled leaves were enclosed in a humidified, close-fitting polyethylene bag at excision and introduced in a polystyrene box. Leaves were placed within the pressure chamber within approximately 1 min after excision. To obtain pressure/volume relationships, leaves were brought to the laboratory and then fully hydrated (C x ]//0.03 MPa) with the cut end of their petioles under water. Fresh mass and C x were taken at intervals during dehydration process (free transpiration technique) until a C x of about /3.5 MPa was reached. The inverse of C x was plotted as a function of the relative water content (RWC). Further details are described in DaMatta et al. [13]. From pressure/volume curves, the osmotic potential (C p) at maximum (C p(max)) and zero (C p(0)) turgor was estimated. Tissue elasticity was characterised using the bulk modulus of elasticity (o ), which was calculated as the slope of the relationship between turgor potential (C p) and RWC [14]. 2.3. Gas exchange Net CO2 assimilation rate (A ), transpiration rate (E ), and stomatal conductance to water vapour (gs) were measured on individual leaves using an LCA-4 portable, open-system infrared gas analyser (Analytical Development Company, Hoddesdon, UK) under natural, saturating photosynthetic photon flux ( /600 mmol m 2 s 1). Leaf chamber conditions tracked ambient air temperatures ranging from 25 to 35 8C over a 4-day
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measuring period. For each selected tree, measurements were made three times during the morning, between 07:30 and 11:30 h, on two different days, so that each set of measurements on each tree was computed as average morning values for gas exchange parameters. Within each treatment-combination, both gs and A did not differ significantly during the morning. 2.4. Total leaf area Four trees per each treatment were randomly selected and completely defoliated on June 6. Total leaf area per tree was measured using an area meter (Area Measurement System, Delta-T Devices, Cambridge, UK). 2.5. Carbon isotope discrimination Nodes were numbered from the apex of plagiotropic branches so that node 1 represented the point of attachment for expanding (c. half final size) leaves, node 2 represented that point for youngest, fully expanded leaves, with increasing node numbers representing successively older leaves. Tissues from leaves of different ages (one leaf per node position per tree) collected on June 6 were oven-dried for 72 h at 60 8C and ground before a combustion at 950 8C under continuous O2 flux. The obtained CO2 was cryogenically purified and its stable isotope composition (13dp) was determined relative to the international PDB standard [15], using a mass spectrometer (Delta-S, Finnigan MAT, Bremen, Germany). Differences in 13dp from duplicates for each sample were below 0.2. Isotope discrimination relative to air (D) was calculated as: 13 da 13 dp ; D 1 13 dp =1000 in which 13da is the carbon isotope composition of the ambient air (assumed to be /8) [6]. 2.6. Statistics The individual tree was considered as the experimental unit. Least significant differences were calculated using appropriate combinations of mean squares and Student’s t-values for the error terms in order to compare clones within irrigation treatments or irrigation treatments within clones at P 5/0.05.
3. Results Xylem pressure potential did not differ between the clone 46 (drought-sensitive) and the clone 120 (droughttolerant) in the irrigated treatment (Table 1). By contrast, Cpd and C md declined significantly under
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Table 1 Xylem water potential measured at predawn (Cpd) and midday (Cmd), osmotic potential at maximum (Cp(max)) and zero (Cp(0)) turgor and bulk volumetric modulus of elasticity (o ) of two field-grown clones of C. canephora grown under irrigated and rainfed conditions Parameters
Cpd (MPa) Cmd (MPa) Cp(max) (MPa) Cp(0) (MPa) o (MPa)
Clone 46
Clone 120
Irrigated
Rainfed
Irrigated
Rainfed
0.05 Aa 0.66 Aa 1.39 Aa 1.75 Aa 8.3 Aa
1.48 Ab 2.66 Ab 2.01 Ab 2.45 Ab 25.1 Ab
0.05 Aa 0.54 Aa 1.72 Aa 2.07 Aa 16.0 Ba
0.60 Bb 1.45 Bb 1.46 Ba 1.88 Ba 12.3 Bb
Different small letters represent statistical significance between means for each parameter within each clone. Different capital letters represent statistical significance between means for each parameter within each watering regime (P 5 0.05, Student’s t -test). Each value represents the mean of six replicates.
rainfed conditions, particularly in clone 46. Compared with unstressed plants, C pd dropped by 0.55 MPa in the clone 120 against 1.43 MPa in the clone 46, while C md decreased by 0.91 MPa in the clone 120 and by 2.0 MPa in the clone 46 (Table 1). Both C p(max) and Cp(0) did not differ significantly between irrigated clones, nor did they change due to drought stress in the clone 120. On the other hand, substantial decreases in both C p(max) (0.62 MPa) and C p(0) (0.70 MPa) were observed in the clone 46 under rainfed conditions (Table 1). This was accompanied by a 3-fold increase in o. In contrast, a 23% drop in o , i.e. increased tissue elasticity, was found in the clone 120 (Table 1). Under irrigation, the clone 120 showed higher gs than the clone 46, but this did not translate into differences between them in A or E , both on a leaf area basis (Table 2). Under rainfed conditions, gs was nearly halved in the clone 120 that was accompanied by a 52% decline in E . In the clone 46, gs did not decrease significantly, though a 39% depression in E was detected. Since E , unlike A , was affected by water stress, an increase in instantaneous WUE, as evaluated by the A /E ratio, was found in both clones (Table 2). A strong decline in total leaf area was observed only in droughted plants of the clone
Fig. 1. Total leaf area of two clones of C. canephora grown under irrigated and rainfed conditions. Bars represent the mean of four replicates. Statistics as in Table 1.
46 (Fig. 1). Leaf fall was preceded by the appearance of chlorotic/necrotic lesions on damaged leaves. Such a phenomenon was apparently negligible in the clone 120. Under irrigated conditions, the clone 120 showed lower D values than the clone 46, thus indicating a higher long-term WUE in the former. Under rainfed conditions, D decreased significantly in both clones, particularly in expanding leaves (Fig. 2). However, absolute values of D were systematically lower in the clone 120 than in the clone 46. It is noteworthy that D increased consistently with increasing leaf age (Fig. 2). For example, irrigated plants of both clones showed an approximate 2.0 change in D when leaves from different positions along the plagiotropic branch were analysed. For droughted clones, such a variation was larger (about 3.5).
Table 2 Average morning values of net CO2 assimilation rate (A ), stomatal conductance to water vapour (gs), transpiration rate (E ) and instantaneous WUE (A /E ) of two field-grown clones of C. canephora grown under irrigated and rainfed conditions Parameters
A (mmol CO2 m 2 s 1) gs (mmol H2O m 2 s 1) E (mmol H2O m 2 s 1) A /E (mmol mol 1) Statistics as in Table 1.
Clone 46
Clone 120
Irrigated
Rainfed
Irrigated
Rainfed
8.5 Aa 54 Aa 1.82 Aa 4.54 Ab
7.9 Aa 48 Aa 1.11 Ab 7.15 Aa
8.9 Aa 79 Ba 1.88 Aa 4.96 Aa
7.5 Aa 39 Ab 0.90 Ab 8.47 Ab
Fig. 2. Carbon isotope discrimination (D) of leaves in relation to their position on a plagiotropic branch of two clones of C. canephora grown under irrigated (solid symbol) and rainfed (open symbol) conditions. Number 1 indicates the node of attachment of expanding leaves (c. half final size), number 2 indicates that node for youngest, expanded leaves, with increasing numbers representing nodes of attachment of successively older leaves. Each symbol is the mean of six replicates; the standard error did not exceed 1.5% of the mean value.
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4. Discussion Under continuous irrigation, there was no difference in water status between the clones (inferred from the very similar values of C pd and C md; Table 1). In addition, instantaneous gas exchange (Table 2) and total leaf area (Fig. 1) were similar in the two clones. When taken together, these facts should explain why their productivities are quite comparable when contrasted under irrigation, as observed in the clonal-test trials by Ferra˜o et al. [11]. In the clone 46, soil drought caused C p(max) and C p(0) to decline markedly together with strong increases in o (Table 1). This indicates an ability for osmotic adjustment, presumably as a consequence of increases in the concentration of solutes. Altogether, these traits should act to decrease the water potential and relative water deficit at zero turgor [16]. In contrast to the results obtained for the clone 46, the clone 120 showed no osmotic adjustment but increased its tissue elasticity under drought stress. For a particular value of C p, increased elasticity facilitates turgor maintenance at lower RWC by effective solute concentration through decreases in cell volume [1,17]. Since the clone 120 showed a lower o , turgor would decline more slowly as dehydration proceeds. Thus, a smaller o or decrease in o would reduce the fluctuation of both cell turgor and C x, and may have ecological significance by buffering plants against short-term changes in water content [18]. By contrast, in plants with a higher o , like the clone 46, C x drops faster during dehydration, thus increasing the soil /plant gradient of water potential and hence water uptake. However, this would be true during morning; an opposite trend would occur in the late afternoon/night, when water potential rises faster due to higher o , thus ultimately reducing water absorption [19,20]. Therefore, total water uptake integrated over a 24-h period would not be as large as often believed in plants with higher o . The clone 46 was not able to compensate for water loss during the day by maintaining water absorption, as based on its considerable more negative Cmd compared with that of the clone 120 (Table 1). Traits such as osmotic adjustment would not be so effective as to sustain water uptake in the long-term in sandy soils as it would be in clay soils under drought stress, by taking into consideration the low waterholding capacity of sandy soils like the one of this study. In this context, a deep rooting would be more advantageous for continued water extraction from drying soils. The clone 120, in turn, had considerably higher C pd and C md than had the clone 46, even though the clone 120 exhibited twice as much the total leaf area of the clone 46 (Fig. 1). Higher C pd and Cmd suggest that the former either or both had a deeper root system to gaining greater access to soil water or depleted accessible soil water more sparingly. Also, less cavitation during the day, since Cx was higher,
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would allow the xylem to refill to a considerable extent during the night. Because of these traits, clone 120 was better able to postpone dehydration, which is why it thrives well on dry, sandy sites [11]. Drought stress induced considerable decrease in total leaf area per tree in the clone 46, but not in the clone 120 (Fig. 1). Though production of new leaves as well as leaf size were not monitored in this study, the large reduction in total leaf area per tree appeared to be mainly resulted from leaf shedding, as observed visually from the extent of defoliation. Stomatal conductance decreased significantly due to drought stress, but only in clone 120. This brought about significant reductions in E per unit leaf area while maintaining A per unit leaf area at comparable rates to those of irrigated plants. Similar behaviour was also observed in the clone 46 (Table 2). Because of the additional resistances associated with CO2 flux into leaves, partial closure of stomata increases the resistance to water movement relatively more than the resistance to CO2 movement, and should reduce E more than it reduces A [21]. Although A at leaf level was nearly constant, it must decrease at whole-tree level in the clone 46 due to the large drop in its total leaf area. Decreases in total leaf area and thus in whole-tree photosynthesis probably account for, at least partially, by the marked reduction in harvestable crop in the clone 46 under rainfed conditions. By contrast, retention of leaves and maintenance of A on a leaf area basis should contribute to reasonably buffer crop yield in the clone 120 against fluctuations in soil water availability. As evidenced by D values, clone 120 showed consistently higher long-term WUE than clone 46. Also, both clones were able to decrease D in response to drought (Fig. 2). Since gas exchange was examined in the shortterm, we cannot speculate about how adjustments in D arose, i.e. whether they resulted predominantly from changes in either gs or A . Whatever the case, our results are in line with those of Meinzer et al. [22]. They showed that field-grown genotypes of Arabica coffee with higher D under full irrigation depleted soil water more rapidly and experienced symptoms of physiological stress earlier when water was withheld, thus indicating that D of wellwatered plants could be used to predict genotype performance under drought stress. One must be cautious, however, since our study was too small to provide a conclusive answer about the usefulness of D as a tool for ranking clones of Robusta coffee with regard to water use. Regardless of the treatments, D increased steadily from the youngest to the oldest leaves along a plagiotropic branch. Similar findings have also been reported for Arabica coffee [23,24]. Such a behaviour should not be attributed to changing irradiance during leaf formation, since coffee leaves develop predominantly at the tips of plagiotropic branches, and hence they experience
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similar irradiances throughout their ontogeny. Adjustments in D are likely to occur as mature, fully expanded leaves became progressively shaded during formation of new leaves. Turn-over of non-cellulose carbon during the process of leaf acclimation to shade should be involved in such an adjustment (see [23] for a more detailed discussion on the matter).
5. Conclusions The present comparative study of clones 46 and 120 revealed them to be similar in several physiological traits when grown under irrigation, but to respond differently to soil drought. In the clone 46, the ability to acclimate to drought via osmotic and tissue rigidity adjustments did not compensate for water loss during the day. Thus, if water availability is restricted, internal water deficits develop and might trigger leaf abscission constraining productivity. By contrast, clone 120 postponed dehydration since it was better able to maintain C x. Its ability to retain leaf area, altogether with maintenance of A per unit leaf area, would help to maintain productivity in seasonally-dry regions that experience satisfactory annual precipitation. In any case, because Robusta coffee is an obligate cross-pollination species, wide population variation in physiological traits to cope with soil drought is to be expected. Although morphological characteristics such as deep rooting, root area, adjustments in root/shoot ratio are not considered in the present study, these are likely also to be important factors for drought tolerance in Robusta coffee and as such merit attention in further research.
Acknowledgements We gratefully acknowledge the Instituto Capixaba de Pesquisa, Assisteˆncia Te´cnica e Extensa˜o Rural (INCAPER) for providing the working facilities. This research was supported by the Conso´rcio Brasileiro de Pesquisa e Desenvolvimento do Cafe´. Research fellowship (F.M. DaMatta) and scholarships (A.R.M. Chaves and H.A. Pinheiro) granted by the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (Brazil) are also acknowledged. Finally, we thank Dr Alisdair Fernie (Max Plank Institute for Molecular Plant Physiology, Germany) for helpful hints in English usage, and two anonymous reviewers for their constructive comments on previous versions of this manuscript.
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[2] T.C. Hsiao, E. Acevedo, E. Fereres, D.W. Henderson, Water stress, growth and osmotic adjustment, Philos. Trans. R. Soc. London Ser. B 273 (1976) 479 /500. [3] N.C. Turner, Further progress in crop water relations, Adv. Agron. 58 (1997) 293 /338. [4] H.G. Jones, Drought tolerance and water-use efficiency, in: J.A.C. Smith, H. Griffiths (Eds.), Water Deficits: Plant Responses from Cell to Community, Bios Scientific Publishers, Oxford, 1993, pp. 193 /201. [5] M. Lauteri, M.C. Scartazza, M.C. Guido, E. Brugnolli, Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments, Funct. Ecol. 11 (1997) 675 /683. [6] G.D. Farquhar, M.H. O’Leary, J.A. Berry, On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves, Aust. J. Plant Physiol. 9 (1982) 121 /137. [7] O.M. Silva, C.A.M. Leite, Competitividade e custos do cafe´ no Brasil e no exterior, in: L. Zambolin (Ed.), Cafe´: Produtividade, Qualidade e Sustentabilidade, Universidade Federal de Vic¸osa, Vic¸osa, 2000, pp. 27 /50. [8] R. Coste, Coffee: The Plant and the Product, MacMillan, London, 1992. [9] K.C. Willson, Coffee, Cocoa and Tea, CABI Publishing, Cambridge, 1999. [10] F.M. DaMatta, A.B. Rena, Toleraˆncia do cafe´ a` seca, in: L. Zambolin (Ed.), Tecnologias de Produc¸a˜o de Cafe´ com Qualidade, Universidade Federal de Vic¸osa, Vic¸osa, 2001, pp. 65 /100. [11] R.G. Ferra˜o, A.F.A. Fonseca, M.A.G. Ferra˜o, L.P. Santos, Comportamento de clones elites de cafe´ Conilon em condic¸o˜es de alta tecnologia no estado do Espı´rito Santo, In: Simpo´sio de Pesquisa dos Cafe´s do Brasil, EMBRAPA, Brası´lia, 2000, pp. 769 /771. [12] R.G. Ferra˜o, A.F.A. Fonseca, M.A.G. Ferra˜o, Avaliac¸a˜o de clones elites de cafe´ Conilon em condic¸a˜o de estresse hı´drico no estado do Espı´rito Santo, In: Simpo´sio de Pesquisa dos Cafe´s do Brasil, EMBRAPA, Brası´lia, 2000, pp. 402 /404. [13] F.M. DaMatta, M. Maestri, R.S. Barros, A.J. Regazzi, Water relations of coffee leaves (Coffea arabica and C. canephora ) in response to drought, J. Hort. Sci. 68 (1993) 741 /746. [14] J.J. Melkonian, J. Wolfe, P.L. Steponkus, Determination of the volumetric modulus of elasticity of wheat leaves by pressure / volume relations and the effects of drought conditioning, Crop Sci. 22 (1982) 116 /123. [15] T.W. Bouttton, Stable carbon isotope ratios of natural materials: sample preparation and mass spectrometric analysis, in: D.C. Coleman, B. Fry (Eds.), Carbon Isotope Techniques, Academic Press, San Diego, 1991, pp. 155 /171. [16] B.M. Pavlik, Seasonal changes of osmotic pressure, symplastic water content and tissue elasticity in the blades of dune grasses growing in situ along the coast of Oregon, Plant Cell Environ. 7 (1984) 531 /539. [17] M.M. Jones, N.C. Turner, Osmotic adjustment in leaves of sorghum in response to water deficits, Plant Physiol. 61 (1978) 122 /126. [18] S. Fan, T.J. Blake, E. Blumwald, The relative contribution of elastic and osmotic adjustments to turgor maintenance in woody species, Physiol. Plant. 90 (1994) 408 /413. [19] P.J. Schulte, The units of currency for plant water status, Plant Cell Environ. 15 (1992) 7 /10. [20] P.J. Schulte, Tissue hydraulic properties and the water relations of desert shrubs, in: J.A.C. Smith, H. Griffiths (Eds.), Water Deficits: Plant Responses from Cell to Community, Bios Scientific Publishers, Oxford, 1993, pp. 177 /192. [21] T.T. Kozlowski, S.G. Pallardy, Physiology of Woody Plants, Academic Press, San Diego, 1997.
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Drought tolerance of two field-grown clones of Coffea canephora Fa´bio M. DaMatta a,*, Agnaldo R.M. Chaves a, Hugo A. Pinheiro a, Carlos Ducatti b, Marcelo E. Loureiro a b
a Departamento de Biologia Vegetal, Universidade Federal de Vic¸osa, 36571-000 Vic¸osa, MG, Brazil Centro de Iso´topos Esta´veis Ambientais, Departamento de Fı´sica e Biofı´sica, Universidade do Estado de Sa˜o Paulo, 18618-000 Botucatu, SP, Brazil
Received 12 March 2002; received in revised form 2 October 2002; accepted 2 October 2002
Abstract We compared tolerance to soil drought of two field-grown clones of Coffea canephora (clone 46, drought-sensitive; and clone 120, drought-tolerant). Under irrigation, there were no marked differences between the clones in water relation parameters, gas exchange and total leaf area. Under rainfed conditions, clone 46 showed osmotic adjustment and increased tissue rigidity. These adjustments, however, were incapable of preventing substantial decreases in xylem pressure potential. By contrast, clone 120 did not exhibit osmotic adjustment, but was able to increase tissue elasticity and to maintain xylem pressure potentials to a greater extent than clone 46 (despite having twice the total leaf area of this clone). Stomatal conductance was lowered by drought in clone 120 but not in clone 46. Carbon assimilation per unit leaf area in both clones remained unaffected under stress. Long-term water use efficiency (WUE), as estimated through carbon isotope discrimination, was consistently greater in clone 120 than in clone 46. Because of these traits, clone 120 was better able to postpone dehydration and to maintain whole-tree photosynthesis. It is proposed that these features should decisively contribute to buffer its productivity in drought-prone areas. # 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Carbon isotope discrimination; Coffea canephora ; Coffee; Drought stress; Gas exchange; Water relations
1. Introduction The ability of a crop to produce satisfactorily in areas subjected to water deficit has been termed drought tolerance regardless of how the ability develops. The mechanisms of drought tolerance have been categorised by Kramer and Boyer [1] as: (i) drought avoidance; (ii) dehydration tolerance; and (iii) dehydration postponement. Some species can avoid drought by maturing rapidly before the onset of dry conditions or reproducing only after rain. Others allow dehydration of the
Abbreviations: A, net carbon assimilation rate; Ci/Ca, ratio of internal to ambient CO2 concentration; E , transpiration rate; gs, stomatal conductance to water vapour; RWC, relative water content; WUE, water use efficiency; D, carbon isotope discrimination; o , bulk leaf modulus of elasticity; C md, midday xylem pressure potential; C p, turgor potential; C pd, predawn xylem pressure potential; Cx, xylem pressure potential; C p, osmotic potential; Cp(max), osmotic potential at maximum turgor; Cp(0), osmotic potential at zero turgor. * Corresponding author. Fax: /55-31-3899-2580 E-mail address: [email protected] (F.M. DaMatta).
tissues and simply tolerate it by continuing to grow when dehydrated or surviving severe dehydration. Still other species can postpone dehydration by growing deep roots and/or effectively controlling water loss chiefly through stomatal closure and decreased leaf area, thus improving plant water status and turgor maintenance. Osmotic adjustment, defined as a net increased solute concentration, can contribute to turgor maintenance and thereby to turgor-mediated processes such as elongation growth and photosynthesis [2]. Although osmotic adjustment may be perceived as a survival mechanism, it does enable physiological activity to be maintained, albeit at a low level throughout a period of water deficit [3]. Turgor maintenance can also be achieved through increases in tissue elasticity, which may permit attainment of a low water potential without the development of detrimental water deficits. By contrast, decreases in tissue elasticity may allow a lower water potential to be reached for a given change in water volume, thus facilitating continued water uptake from drying soil [1].
0168-9452/02/$ - see front matter # 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 8 - 9 4 5 2 ( 0 2 ) 0 0 3 4 2 - 4
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Water use efficiency (WUE), defined as the ratio of carbon gain to water loss, is thought to play an important role in acclimation, productivity and the probability of survival under drought stress [4,5]. Plants can achieve a high WUE through either a high rate of net carbon assimilation (A ) or a low rate of transpiration (E ), or both. In C3 plants, the stable carbon isotope discrimination (D) is related to whole-plant WUE through, amongst other factors, the stomatal control of gas exchange and the degree of discrimination against 13 C with changing ratio of internal to ambient CO2 concentrations, Ci/Ca [6]. Typically, plants with a favourable water status have a high Ci/Ca and are depleted in 13C, whereas droughted plants have a low Ci/Ca and are enriched in 13C, reflecting the trade-off between A and E . From about 90 species of Coffea , only Coffea arabica (Arabica coffee) and Coffea canephora (Robusta coffee) are significant in the world commercial trade. The volume of business generated from Robusta coffee on the international coffee market has been steadily increasing for half a century, and presently this species accounts for about one-third of the coffee consumed world-wide [7]. Robusta coffee is native to lowland forest of the Congo river basin (Africa) with a typical equatorial climate in which average temperature is between 24 and 26 8C and an abundant rainfall distributed over a 9 /10-month period, and atmospheric humidity at a nearly constant level approaching saturation [8,9]. Under plantation schemes, a necessary minimum annual rainfall of 1250 mm, or even 1550 mm, has been quoted, but this would require an even distribution [8]. In the main Brazilian area producing Robusta coffee (Espı´rito Santo State), there is an increasing trend in expanding cultivation towards marginal and degraded lands where water availability constitutes one of the major problems. In these areas, during the dry season, which lasts from 4 to 7 months, evaporation by far exceeds rainfall and, within the rainy season, rainfall pattern and amount are to a great extent unpredictable. Such conditions could be expected to largely restrict the productive potential of Robusta coffee. Local experience has shown that crop yield under rainfed conditions may decrease by about 40% or even as much as by 80% in dry years. Irrigation has been successfully employed, enabling the plant to be a profitable crop and preventing crop failure in dry years. However, costs involved for purchasing and installing irrigation equipment are rather expensive and immediately pose a problem for the profitability of its use, particularly in small farms where Robusta coffee is mostly cultivated. In addition, a permanent, reliable source of water for irrigation is not always available. Over the last 15 years vegetative methods of selection have improved significantly the clonal performance of
Robusta coffee under drought conditions, rendering coffee cropping less dependent on irrigation. Clones were originally selected from commercial, open-pollinated plantations from Espı´rito Santo State by visual assessment of trees with suspected superior performance under certain climatic conditions. However, performance has been evaluated exclusively in terms of harvestable crop, without examination of how physiological parameters may contribute to drought tolerance in this species [10]. In this work, we have evaluated two highly productive clones when grown under irrigation; under limited soil water, however, both survival and productivity are severely impaired in the droughtsensitive clone, while only marginal effects on productivity have been noted to occur in the drought-tolerant clone [11,12]. A major goal of this study was to physiologically examine how these clones respond to soil drought in order to explain the differences in their yield responses.
2. Material and methods 2.1. General The study site is located in the Experimental Station of Sooretama (19824?S, 40831W, 30 m elevation), Espı´rito Santo State, south-eastern Brazil. The soil at the site is a flat, deep, sandy Oxisol with a volumetric water content 15.7% at field capacity and 8.3% at permanent wilting point; it is extensively found in areas of cultivation of Robusta coffee in that region. The site receives an average annual rainfall of 1200 mm with a marked dry season from March/April to September/ October. Average annual temperature is 23.5 8C. Uniform seedlings of two clones of C. canephora Pierre var. Conillon (clone 46, drought-sensitive; and clone 120, drought-tolerant) with four leaf pairs, obtained as rooted stem cuttings, were planted in two adjacent plots in April 1996 at a spacing of 2.5 m between rows and 1.0 m within rows. During the first 2 years after planting, all trees were irrigated equally to guarantee the uniformity of plant development. Irrigation, applied by overhead sprinklers, was scheduled whenever potential soil water deficit reached 20 mm, as estimated from pan evaporation. The trees were trained with four heads and received routine agricultural practices suitable for commercial bean production including hoeing, fertilisation and chemical control of insect and pathogen attack. After late March 1998, one plot was maintained without any irrigation (rainfed conditions) while the other continued receiving irrigation as outlined above. From April through September 1998 there was no appreciable rainfall. Field measurements were conducted on cloudless days from June 02 to 06, 1998, starting 55 days after last rainfall. Compara-
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tively, clone 46 has larger leaves, shorter internodes, shorter plagiotropic branches and slightly denser crowns than clone 120. No significant difference in plant height was observed between the clones, regardless of the watering regime. Probably, the rainless period was not long enough to lead to reductions in height in rainfed plants. Unless otherwise stated, sampling and measurements were made on six trees randomly chosen per each clone selected within each water regime, using the youngest, fully expanded, upper-canopy, sunlit leaves (one leaf per tree). Measurements of xylem pressure potential (C x) and gas exchange for each tree were repeated once in another day; for data analysis, observations on each day were treated as subsamples. Environmental conditions of humidity, air temperature and solar radiation, as monitored by a meteorological station localised in the Experimental Station, did not differ significantly among the measurement days. Thus, day-to-day variation in those measurements was assumed to reflect differences in both clonal and irrigation treatments. 2.2. Water relations Leaf C x was measured in the field at both predawn (C pd) and midday (C md) using a Scholander-type pressure chamber. The sampled leaves were enclosed in a humidified, close-fitting polyethylene bag at excision and introduced in a polystyrene box. Leaves were placed within the pressure chamber within approximately 1 min after excision. To obtain pressure/volume relationships, leaves were brought to the laboratory and then fully hydrated (C x ]//0.03 MPa) with the cut end of their petioles under water. Fresh mass and C x were taken at intervals during dehydration process (free transpiration technique) until a C x of about /3.5 MPa was reached. The inverse of C x was plotted as a function of the relative water content (RWC). Further details are described in DaMatta et al. [13]. From pressure/volume curves, the osmotic potential (C p) at maximum (C p(max)) and zero (C p(0)) turgor was estimated. Tissue elasticity was characterised using the bulk modulus of elasticity (o ), which was calculated as the slope of the relationship between turgor potential (C p) and RWC [14]. 2.3. Gas exchange Net CO2 assimilation rate (A ), transpiration rate (E ), and stomatal conductance to water vapour (gs) were measured on individual leaves using an LCA-4 portable, open-system infrared gas analyser (Analytical Development Company, Hoddesdon, UK) under natural, saturating photosynthetic photon flux ( /600 mmol m 2 s 1). Leaf chamber conditions tracked ambient air temperatures ranging from 25 to 35 8C over a 4-day
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measuring period. For each selected tree, measurements were made three times during the morning, between 07:30 and 11:30 h, on two different days, so that each set of measurements on each tree was computed as average morning values for gas exchange parameters. Within each treatment-combination, both gs and A did not differ significantly during the morning. 2.4. Total leaf area Four trees per each treatment were randomly selected and completely defoliated on June 6. Total leaf area per tree was measured using an area meter (Area Measurement System, Delta-T Devices, Cambridge, UK). 2.5. Carbon isotope discrimination Nodes were numbered from the apex of plagiotropic branches so that node 1 represented the point of attachment for expanding (c. half final size) leaves, node 2 represented that point for youngest, fully expanded leaves, with increasing node numbers representing successively older leaves. Tissues from leaves of different ages (one leaf per node position per tree) collected on June 6 were oven-dried for 72 h at 60 8C and ground before a combustion at 950 8C under continuous O2 flux. The obtained CO2 was cryogenically purified and its stable isotope composition (13dp) was determined relative to the international PDB standard [15], using a mass spectrometer (Delta-S, Finnigan MAT, Bremen, Germany). Differences in 13dp from duplicates for each sample were below 0.2. Isotope discrimination relative to air (D) was calculated as: 13 da 13 dp ; D 1 13 dp =1000 in which 13da is the carbon isotope composition of the ambient air (assumed to be /8) [6]. 2.6. Statistics The individual tree was considered as the experimental unit. Least significant differences were calculated using appropriate combinations of mean squares and Student’s t-values for the error terms in order to compare clones within irrigation treatments or irrigation treatments within clones at P 5/0.05.
3. Results Xylem pressure potential did not differ between the clone 46 (drought-sensitive) and the clone 120 (droughttolerant) in the irrigated treatment (Table 1). By contrast, Cpd and C md declined significantly under
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Table 1 Xylem water potential measured at predawn (Cpd) and midday (Cmd), osmotic potential at maximum (Cp(max)) and zero (Cp(0)) turgor and bulk volumetric modulus of elasticity (o ) of two field-grown clones of C. canephora grown under irrigated and rainfed conditions Parameters
Cpd (MPa) Cmd (MPa) Cp(max) (MPa) Cp(0) (MPa) o (MPa)
Clone 46
Clone 120
Irrigated
Rainfed
Irrigated
Rainfed
0.05 Aa 0.66 Aa 1.39 Aa 1.75 Aa 8.3 Aa
1.48 Ab 2.66 Ab 2.01 Ab 2.45 Ab 25.1 Ab
0.05 Aa 0.54 Aa 1.72 Aa 2.07 Aa 16.0 Ba
0.60 Bb 1.45 Bb 1.46 Ba 1.88 Ba 12.3 Bb
Different small letters represent statistical significance between means for each parameter within each clone. Different capital letters represent statistical significance between means for each parameter within each watering regime (P 5 0.05, Student’s t -test). Each value represents the mean of six replicates.
rainfed conditions, particularly in clone 46. Compared with unstressed plants, C pd dropped by 0.55 MPa in the clone 120 against 1.43 MPa in the clone 46, while C md decreased by 0.91 MPa in the clone 120 and by 2.0 MPa in the clone 46 (Table 1). Both C p(max) and Cp(0) did not differ significantly between irrigated clones, nor did they change due to drought stress in the clone 120. On the other hand, substantial decreases in both C p(max) (0.62 MPa) and C p(0) (0.70 MPa) were observed in the clone 46 under rainfed conditions (Table 1). This was accompanied by a 3-fold increase in o. In contrast, a 23% drop in o , i.e. increased tissue elasticity, was found in the clone 120 (Table 1). Under irrigation, the clone 120 showed higher gs than the clone 46, but this did not translate into differences between them in A or E , both on a leaf area basis (Table 2). Under rainfed conditions, gs was nearly halved in the clone 120 that was accompanied by a 52% decline in E . In the clone 46, gs did not decrease significantly, though a 39% depression in E was detected. Since E , unlike A , was affected by water stress, an increase in instantaneous WUE, as evaluated by the A /E ratio, was found in both clones (Table 2). A strong decline in total leaf area was observed only in droughted plants of the clone
Fig. 1. Total leaf area of two clones of C. canephora grown under irrigated and rainfed conditions. Bars represent the mean of four replicates. Statistics as in Table 1.
46 (Fig. 1). Leaf fall was preceded by the appearance of chlorotic/necrotic lesions on damaged leaves. Such a phenomenon was apparently negligible in the clone 120. Under irrigated conditions, the clone 120 showed lower D values than the clone 46, thus indicating a higher long-term WUE in the former. Under rainfed conditions, D decreased significantly in both clones, particularly in expanding leaves (Fig. 2). However, absolute values of D were systematically lower in the clone 120 than in the clone 46. It is noteworthy that D increased consistently with increasing leaf age (Fig. 2). For example, irrigated plants of both clones showed an approximate 2.0 change in D when leaves from different positions along the plagiotropic branch were analysed. For droughted clones, such a variation was larger (about 3.5).
Table 2 Average morning values of net CO2 assimilation rate (A ), stomatal conductance to water vapour (gs), transpiration rate (E ) and instantaneous WUE (A /E ) of two field-grown clones of C. canephora grown under irrigated and rainfed conditions Parameters
A (mmol CO2 m 2 s 1) gs (mmol H2O m 2 s 1) E (mmol H2O m 2 s 1) A /E (mmol mol 1) Statistics as in Table 1.
Clone 46
Clone 120
Irrigated
Rainfed
Irrigated
Rainfed
8.5 Aa 54 Aa 1.82 Aa 4.54 Ab
7.9 Aa 48 Aa 1.11 Ab 7.15 Aa
8.9 Aa 79 Ba 1.88 Aa 4.96 Aa
7.5 Aa 39 Ab 0.90 Ab 8.47 Ab
Fig. 2. Carbon isotope discrimination (D) of leaves in relation to their position on a plagiotropic branch of two clones of C. canephora grown under irrigated (solid symbol) and rainfed (open symbol) conditions. Number 1 indicates the node of attachment of expanding leaves (c. half final size), number 2 indicates that node for youngest, expanded leaves, with increasing numbers representing nodes of attachment of successively older leaves. Each symbol is the mean of six replicates; the standard error did not exceed 1.5% of the mean value.
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4. Discussion Under continuous irrigation, there was no difference in water status between the clones (inferred from the very similar values of C pd and C md; Table 1). In addition, instantaneous gas exchange (Table 2) and total leaf area (Fig. 1) were similar in the two clones. When taken together, these facts should explain why their productivities are quite comparable when contrasted under irrigation, as observed in the clonal-test trials by Ferra˜o et al. [11]. In the clone 46, soil drought caused C p(max) and C p(0) to decline markedly together with strong increases in o (Table 1). This indicates an ability for osmotic adjustment, presumably as a consequence of increases in the concentration of solutes. Altogether, these traits should act to decrease the water potential and relative water deficit at zero turgor [16]. In contrast to the results obtained for the clone 46, the clone 120 showed no osmotic adjustment but increased its tissue elasticity under drought stress. For a particular value of C p, increased elasticity facilitates turgor maintenance at lower RWC by effective solute concentration through decreases in cell volume [1,17]. Since the clone 120 showed a lower o , turgor would decline more slowly as dehydration proceeds. Thus, a smaller o or decrease in o would reduce the fluctuation of both cell turgor and C x, and may have ecological significance by buffering plants against short-term changes in water content [18]. By contrast, in plants with a higher o , like the clone 46, C x drops faster during dehydration, thus increasing the soil /plant gradient of water potential and hence water uptake. However, this would be true during morning; an opposite trend would occur in the late afternoon/night, when water potential rises faster due to higher o , thus ultimately reducing water absorption [19,20]. Therefore, total water uptake integrated over a 24-h period would not be as large as often believed in plants with higher o . The clone 46 was not able to compensate for water loss during the day by maintaining water absorption, as based on its considerable more negative Cmd compared with that of the clone 120 (Table 1). Traits such as osmotic adjustment would not be so effective as to sustain water uptake in the long-term in sandy soils as it would be in clay soils under drought stress, by taking into consideration the low waterholding capacity of sandy soils like the one of this study. In this context, a deep rooting would be more advantageous for continued water extraction from drying soils. The clone 120, in turn, had considerably higher C pd and C md than had the clone 46, even though the clone 120 exhibited twice as much the total leaf area of the clone 46 (Fig. 1). Higher C pd and Cmd suggest that the former either or both had a deeper root system to gaining greater access to soil water or depleted accessible soil water more sparingly. Also, less cavitation during the day, since Cx was higher,
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would allow the xylem to refill to a considerable extent during the night. Because of these traits, clone 120 was better able to postpone dehydration, which is why it thrives well on dry, sandy sites [11]. Drought stress induced considerable decrease in total leaf area per tree in the clone 46, but not in the clone 120 (Fig. 1). Though production of new leaves as well as leaf size were not monitored in this study, the large reduction in total leaf area per tree appeared to be mainly resulted from leaf shedding, as observed visually from the extent of defoliation. Stomatal conductance decreased significantly due to drought stress, but only in clone 120. This brought about significant reductions in E per unit leaf area while maintaining A per unit leaf area at comparable rates to those of irrigated plants. Similar behaviour was also observed in the clone 46 (Table 2). Because of the additional resistances associated with CO2 flux into leaves, partial closure of stomata increases the resistance to water movement relatively more than the resistance to CO2 movement, and should reduce E more than it reduces A [21]. Although A at leaf level was nearly constant, it must decrease at whole-tree level in the clone 46 due to the large drop in its total leaf area. Decreases in total leaf area and thus in whole-tree photosynthesis probably account for, at least partially, by the marked reduction in harvestable crop in the clone 46 under rainfed conditions. By contrast, retention of leaves and maintenance of A on a leaf area basis should contribute to reasonably buffer crop yield in the clone 120 against fluctuations in soil water availability. As evidenced by D values, clone 120 showed consistently higher long-term WUE than clone 46. Also, both clones were able to decrease D in response to drought (Fig. 2). Since gas exchange was examined in the shortterm, we cannot speculate about how adjustments in D arose, i.e. whether they resulted predominantly from changes in either gs or A . Whatever the case, our results are in line with those of Meinzer et al. [22]. They showed that field-grown genotypes of Arabica coffee with higher D under full irrigation depleted soil water more rapidly and experienced symptoms of physiological stress earlier when water was withheld, thus indicating that D of wellwatered plants could be used to predict genotype performance under drought stress. One must be cautious, however, since our study was too small to provide a conclusive answer about the usefulness of D as a tool for ranking clones of Robusta coffee with regard to water use. Regardless of the treatments, D increased steadily from the youngest to the oldest leaves along a plagiotropic branch. Similar findings have also been reported for Arabica coffee [23,24]. Such a behaviour should not be attributed to changing irradiance during leaf formation, since coffee leaves develop predominantly at the tips of plagiotropic branches, and hence they experience
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similar irradiances throughout their ontogeny. Adjustments in D are likely to occur as mature, fully expanded leaves became progressively shaded during formation of new leaves. Turn-over of non-cellulose carbon during the process of leaf acclimation to shade should be involved in such an adjustment (see [23] for a more detailed discussion on the matter).
5. Conclusions The present comparative study of clones 46 and 120 revealed them to be similar in several physiological traits when grown under irrigation, but to respond differently to soil drought. In the clone 46, the ability to acclimate to drought via osmotic and tissue rigidity adjustments did not compensate for water loss during the day. Thus, if water availability is restricted, internal water deficits develop and might trigger leaf abscission constraining productivity. By contrast, clone 120 postponed dehydration since it was better able to maintain C x. Its ability to retain leaf area, altogether with maintenance of A per unit leaf area, would help to maintain productivity in seasonally-dry regions that experience satisfactory annual precipitation. In any case, because Robusta coffee is an obligate cross-pollination species, wide population variation in physiological traits to cope with soil drought is to be expected. Although morphological characteristics such as deep rooting, root area, adjustments in root/shoot ratio are not considered in the present study, these are likely also to be important factors for drought tolerance in Robusta coffee and as such merit attention in further research.
Acknowledgements We gratefully acknowledge the Instituto Capixaba de Pesquisa, Assisteˆncia Te´cnica e Extensa˜o Rural (INCAPER) for providing the working facilities. This research was supported by the Conso´rcio Brasileiro de Pesquisa e Desenvolvimento do Cafe´. Research fellowship (F.M. DaMatta) and scholarships (A.R.M. Chaves and H.A. Pinheiro) granted by the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (Brazil) are also acknowledged. Finally, we thank Dr Alisdair Fernie (Max Plank Institute for Molecular Plant Physiology, Germany) for helpful hints in English usage, and two anonymous reviewers for their constructive comments on previous versions of this manuscript.
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