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Revista Brasileira de Fisiologia Vegetal

Print version ISSN 0103-3131

Rev. Bras. Fisiol. Veg. vol.13 no.1 Lavras  2001 




Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36571-000 Viçosa, MG, Brasil



ABSTRACT - The actual (A) and potential (Apot) photosynthetic rates of C3 and C4 tropical crop species grown under greenhouse conditions was compared. The following species were investigated: Oryza sativa, Phaseolus vulgaris, Glycine max, Helianthus annuus, Gossypium hirsutum, Manihot esculenta, Theobroma cacao, Coffea arabica, Hevea brasiliensis, and Eucalyptus urophylla × E. grandis, all from the C3 group, and Amaranthus sp., Panicum maximum, Pennisetum purpureum, Zea mays and Saccharum officinarum, from the C4 group. A, determined under non-limiting light at ambient temperature and CO2, was measured with an infrared gas analyser, whilst Apot, determined under saturating light and CO2 at an optimal temperature (35 oC for all species), was gauged with a gas-phase  oxygen electrode. On an area basis, A varied from 5.0 up to 26.3 mmol CO2 m-2 s-1, whilst Apot was very similar in 14 of the 15 species, with an average rate of 35.0 ± 2.4 mmol O2 m-2 s-1. The value of Apot in T. cacao was approximately half the mean of the remaining species. On a mass basis, variations in A were much larger, and differences in Apot, although not large, emerged. The overall mean Apot per unit mass in the four tree species was 28.0 ± 2.2 mmol O2 g-1 min-1 against 44.6 ± 5.8 mmol O2 g-1 min-1 in the remaining species. As a whole, the results evidenced a conservative behaviour of the photosynthetic apparatus to fix CO2 amongst the species investigated, despite the large differences in A among them.
ADDITIONAL INDEX TERMS: Carbon assimilation rate, photosynthetic oxygen evolution, specific leaf area.


RESUMO – Compararam-se as taxas fotossintéticas atual (A) e potencial (Apot) de espécies tropicais C3 e C4 cultivadas sob condições de casa-de-vegetação. Foram estudadas as seguintes espécies: Oryza sativa, Phaseolus vulgaris, Glycine max, Helianthus annuus, Gossypium hirsutum, Manihot esculenta, Theobroma cacao, Coffea arabica, Hevea brasiliensis, e Eucalyptus urophylla × E. grandis, todas do grupo C3, e Amaranthus sp., Panicum maximum, Pennisetum purpureum, Zea mays e Saccharum officinarum, do grupo C4. A, determinada sob alta irradiância e temperatura e CO2 ambientes, foi medida com um analisador de gases a infravermelho, enquanto Apot, determinada sob luz e CO2 saturantes e à temperatura ótima (35 oC para todas as espécies), foi medida com um eletrodo de oxigênio de fase gasosa. Em base de área, A variou desde 5,0 até 26,3 mmol CO2 m-2 s-1, enquanto Apot foi similar em 14 das 15 espécies avaliadas, com uma taxa média de 35.0 ± 2.4 mmol O2 m-2 s-1. Observou-se um padrão diferencial em T. cacao, em que Apot decresceu, aproximadamente, em 50% em relação a Apot das demais espécies estudadas. Em base de massa, as variações em A foram bem maiores e diferenças em Apot, embora não expressivas, puderam ser observadas. Os valores médios de Apot por unidade de massa, nas quatro espécies lenhosas, foi 28.0 ± 2.2 mmol O2 g-1 min-1, contra 44.6 ± 5.8 mmol O2 g-1 min-1 nas espécies remanescentes. Como um todo, os resultados evidenciaram um comportamento conservado do aparelho fotossintético, em termos de fixação do CO2, nas espécies estudadas, a despeito das largas diferenças em A entre elas.
TERMOS ADICIONAIS PARA INDEXAÇÃO: Área foliar específica, evolução do oxigênio fotossintético, taxa de assimilação do carbono.




Large differences in the actual photosynthetic rates (A), termed herein as the maximum net rate of carbon uptake under non-limiting photosynthetic photon flux (PPF) at ambient temperature and CO2 in healthy, unstressed plants, exist within the plant kingdom. On an area basis, values of A cover a wide range, from less than 2 up to 70 mmol CO2 m-2 s-1 (Larcher, 1995), and may even achieve values as high as 80 mmol CO2 m-2 s-1, as in Amaranthus retroflexus (Pearcy and Ehleringer, 1984). However, it is often difficult to make meaningful comparisons of photosynthetic rates as determined by different investigators because of variations in measurement techniques and methods of expressing photosynthetic rates, in addition to preconditioning effects of environment on leaf anatomy (Kozlowski and Pallardy, 1997).

Comparative studies of C3 and C4 plants have generally shown that the latter, in their native habitats, exhibit higher photosynthetic rates. Such a behaviour is largely a result of a suite of biochemical, physiological and morphological components collectively functioning to concentrate CO2 in vascular bundle sheath cells (Pearcy and Ehleringer, 1984). On the other hand, the majority of C3 plants, particularly woody species, display low photosynthetic performances (Körner, 1995; Larcher, 1995). However, some agricultural C3 crop plants may achieve photosynthetic rates near or similar to those of C4 species, possibly due to successful breeding (Larcher, 1995). On biochemical grounds, the causes of the specific differences in A lie in the capacity of ribulose-1,5-bisphosphate (RuBP) carboxylase to consume RuBP, the capacity of the thylakoid and Calvin cycle reactions to regenerate RuBP, and the capacity of starch and sucrose synthesis to regenerate inorganic phosphate from phosphorylated photosynthetic intermediates. Each of these processes represents major points of direct interaction with the environment beyond the photosynthetic apparatus (Sage and Reid, 1994).

Some investigations have been conducted in order to characterise the photosynthetic performance of a given species or a community. In several cases a high correlation between leaf nitrogen concentration and A of different species has been found (Field and Mooney, 1986; Chazdon and Field, 1987; Evans, 1989; Reich and Walters, 1994; Woodward and Smith, 1995). Other studies have shown a high correlation between leaf conductance and A within diverse vegetation types distributed world-wide (Körner et al., 1979; Körner, 1995). Comparatively with A, to our knowledge less is known about the characterisation of potential photosynthetic rates (Apot), which herein represent the rate of net photosynthesis as measured at optimal temperature under saturating PPF and CO2. Previous results obtained in our laboratory with some tropical species revealed very similar values of Apot among species, despite large differences in A among them. It remains to be ascertained, therefore, whether Apot shows a conservative pattern among plants of different photosynthetic performances. In this preliminary work, A and Apot were measured in 14 C3 and C4 tropical crop species, including herbaceous and woody plants which differ widely in growth habit, leaf anatomy and photosynthetic capacity. For comparison, a C4 dicot, Amaranthus sp., a weed plant commonly occurring in disturbed habitats and agricultural fields, was also investigated.



Plant material and growth conditions

Photosynthetic measurements were conducted on ten C3 species, including one monocot, rice (Oryza sativa L.), four herbaceous dicots, common bean (Phaseolus vulgaris L.), soybean (Glycine max [L.] Merr.), sunflower (Helianthus annuus L.) and cotton (Gossypium hirsutum L.), one shrub, cassava (Manihot esculenta Crantz), and four tree dicot plants, cacao (Theobroma cacao L.), coffee (Coffea arabica L.), rubber (Hevea brasiliensis [H.B.K.] Muell-Arg.) and eucalyptus (Eucalyptus urophylla Blake × E. grandis Hill ex Maiden). Five C4 species were also used, including one dicot, pigweed (Amaranthus sp.), and four monocots, panic grass (Panicum maximum Jacq.), millet (Pennisetum purpureum Schumach), maize (Zea mays L.) and sugarcane (Saccharum officinarum L.). Eucalyptus, cassava and sugarcane were grown from stem cuttings, and the remaining species were raised from seeds.

The experiment was carried out in Viçosa (20o45’S, 650 m a.s.l.), Brazil, in a greenhouse at ambient CO2 without temperature control. At 13h00, air temperature inside the greenhouse was up to 7 oC higher than outside air. Incoming PPF was transmitted by 60%, as determined in mid-summer. Plants were grown in 6-L plastic pots containing a 3:1 (v:v) mixture of soil and manure. In order to get uniform plants, the seedlings were thinned after germination. Plants were watered daily and flushed once a week with 400 mL of full strength Hoagland solution (Hoagland and Arnon, 1950). At the time of measurements, the herbaceous plants, employed prior to flowering, were four to six weeks old, and the young tree species were eight to 13 months old. Cassava was approximately two months old. All measurements were made in late spring or in summer on a youngest, completely expanded mature leaf or leaflet.

Leaf gas exchange parameters

The stomatal conductance to water vapour (gs) and A were measured on attached leaves at ambient CO2 partial pressure (about 36 Pa) using a portable, open-system infrared gas analyser (LCA-4, Analytical Development Co., Hoddesdon, UK). Artificial PPF was supplied by a portable light unit (PLU2-002) containing a dichroic 12 V, 20 W lamp, an air extractor fan and an infrared heat absorbing filter. For C3 species, PPF for saturating photosynthesis was determined from response curves of A to PPF obtained in triplicates for each species; such a saturating PPF varied from 650-750 mmol m-2 s-1 as in cacao and coffee, respectively, to 1700 mmol m-2 s-1 as in sunflower. For C4 species, photosynthesis was not fully saturated by employing the maximum attainable PPF of almost 2000 mmol m-2 s-1. After fitting the leaf tissue in the Parckinson leaf chamber (PLC4), rates for gas exchange were typically settled within 2-3 min, nearly paralleling stabilisation for internal CO2 values. Gas flow through the leaf chamber was 255 ± 2 mmol s-1. During the measurements (08h30-09h30), the air relative humidity and leaf temperature ranged from 74 to 83%, and 24 to 29oC, respectively.

Potential photosynthetic rates (Apot) were measured by oxygen evolution on the same leaves used for A measurements, and determined under saturating CO2 partial pressure (approximately 5 kPa supplied by 0.2 mL of 1 kmol m-3 KHCO3), using a gas-phase oxygen electrode (LD-2 Leaf Chamber, Hansatech, Norfolk, UK). PPF was provided by a 200 W halogen-tungsten bulb mounted in a light source (LS2, Hansatech), which gave little less than 3000 mmol m-2 s-1. Saturating PPF at the leaf  disk surface (1500-2600 mmol m-2 s-1) was adjusted by using neutral density filters. Maximum values of Apot were measured at 35 oC following response curves of Apot to temperature obtained in triplicates for all species. Photosynthetic rates were also measured at saturating light and CO2, but at the same average leaf temperature at which A was measured (Amax). When possible, Amax and Apot were determined in 10 cm2 leaf discs; in other cases leaf slices were used, and their total area for photosynthetic rate calculations was measured using an area meter (Area Measurement System, Delta-T Devices, Cambridge, UK). Leaf pieces were then dried to constant mass at 70 oC in order to determine their specific leaf area (SLA). This parameter was used to express photosynthetic rates per unit mass.

Statistical analysis

Statistical significance among means obtained from 12 replicates was determined using an ANOVA analysis with a Newman-Keuls’ post-test to examine if significant (P < 0.05) differences occurred between individual means. In some cases, non-orthogonal contrasts were used in order to confront the overall means from certain groups of plants (e.g., woody species against the remaining ones) using a Scheffé’s test.



As Table 1 shows, A per unit area varied widely among the species investigated, from 5.0 up to 26.3 mmol CO2 m-2 s-1. As expected, C4 plants exhibited the greatest values of A, although sunflower had values similar to plants of the C4 group, likely as a result of its high gs (Table 1) and high amounts of Rubisco (Larcher, 1995). Tree species showed the lowest A; in eucalyptus, however, A laid in the range of herbaceous C3 plants, probably as a consequence of its unusually large gs (Table 1). Differences in A, particularly amongst the C3 plants, might be to some extent attributed to differences in gs. Nonetheless, values of A, particularly for C4 species, were in general lower than those reported elsewhere (e.g., Gifford, 1974; Ziska and Bunce, 1997). This might in part be a consequence of relatively high temperatures inside the greenhouse.



When rates of photosynthesis were measured at saturating CO2 (Amax), a different pattern emerged (Table 1). In general, the differences in Amax amongst species were quite narrow, and hence variations in Amax/A ratio were due chiefly to changes in A. In C4 plants that ratio ranged from 1.05 to 1.12, indicating that photosynthesis is almost saturated at ambient CO2. In C3 species Amax/A ratio laid between 1.31 and 5.40 (Table 1). In other words, the rates of photosynthesis under saturating CO2 could be up to 440% above those found at current atmospheric CO2 partial pressure, as was the case of rubber seedlings. Because Amax was determined under saturating CO2, minimal or no limitation to CO2 diffusion from the outside atmosphere to the carboxylation sites in the chloroplasts and the inhibition of photorespiration are to be expected. These facts undoubtedly contributed to the similarity of values of Amax observed among the species investigated.

It should be stressed that slight differences in leaf temperature between measurements of A and Amax occurred and therefore the values of these parameters among the species examined might not be rigorously comparable. Regardless of the wide variations in A, Apot (measured at 35 oC) per unit area was very similar for all species except for cacao, in which it was significantly lowered (42%; P < 0.0001) than the overall mean Apot (35 ± 2.4 mmol O2 m-2 s-1) of the remaining 14 species (Table 1). The results obtained with cacao should, however, be interpreted cautiously because, as opposed to the other species, cacao seedlings display several shade adaptation attributes. For example, although being cultivated under the same light regime, cacao leaves showed a significant (P < 0.0001) doubling in SLA in comparison with the mean SLA from the other three tree species (Table 2). Thus, it is, possible that the differential behaviour of Apot in cacao might be a consequence of its native origin and domestication as understory, shade trees which commonly exhibit low light-saturated photosynthetic rates as a result of low concentration of photosynthetic enzymes and electron transport carriers per unit area (Chazdon et al., 1996). Coffee, on the other hand, in spite of its being originated in natural shady habitats, has a high photosynthetic plasticity, being successfully cultivated at full sun, as in Brazil. With the exception of Apot for cacao plants, the present results suggest that the photosynthetic potential of individual leaves on an area basis might be a conservative attribute amongst the tropical species here investigated. This pattern should not be attributed to inhibitory effects of high CO2 on respiration (Saralabai et al., 1997), or to respiration per se, as no consistent difference in respiratory rates under either normal or high CO2 was found amongst the species studied (not shown). Although the results obtained here refer to only one developmental stage under one set of growth conditions, in a side experiment the overall rate of Apot per unit area of field-grown panic grass, millet, sugarcane, pigweed, cassava, coffee and rubber tree was 34.8 ± 3.9 mmol O2 m2 s-1, within the same range of values of the present study. A similar rate with hydroponically-cultured common bean at pod formation stage was also found (Lima et al., 2000), supporting the suggestion of a conservative behaviour of Apot.



The most satisfactory basis for expressing photosynthetic rates apparently is leaf area (Kramer and Kozlowski, 1979). However, area-based photosynthesis may be misleading because thick leaves may have more chloroplasts per unit surface than thin leaves; therefore a high rate of CO2 uptake per unit area would be expected, regardless of what would cause the difference in thickness (Kramer and Kozlowski, 1979; Brown, 1994). In fact, mass-based photosynthesis and SLA are usually negatively related to each other (Reich et al., 1991; Prado and Moraes, 1997). Hence, the variations in A per unit area in the present work, in addition to those attributable to gs, could have arisen in part from differences in SLA (Table 2). Nonetheless, A per unit area and SLA showed a trend to change in the same  direction,  although   the  correlation between these parameters was not significant (P > 0.05). By expressing A per unit mass (Table 3), the differences in photosynthetic rates among species were markedly larger than those of A per unit area. On the other hand, the variations of Apot per unit mass were not so large, with a little more than a doubling between the lowest and the highest value of Apot obtained with rubber tree and sunflower, respectively (Table 3). Again, this fact also lends support to the hypothesis that Apot, whether considered on either an area or a mass basis, is a conservative attribute in the species investigated.



By contrasting the tree species with the remaining ones, mass-based Apot was significantly (P < 0.001) lower in the tree species, these producing an overall Apot of 28.0 ± 2.2 mmol O2 g-1 min-1 against 44.6 ± 5.8 mmol O2 g-1 min-1 for the other species. This difference was markedly associated with the low SLA in tree species (except cacao). It should be emphasised, however, that low SLA,  particularly  in  woody  plants,  could  result from an increased investment in non-photosynthetic tissues throughout their long leaf life-spans (Bongers and Popma, 1990; Reich and Walters, 1994).

In addition, lower SLA and longer leaf life-span have been also associated with (1) potentially different infra-leaf allocation of nitrogen; (2)  greater  within-leaf  shading;  and (3) potential diffusion limitations to net carbon uptake (Poorter and Evans, 1998; Reich et al., 1998). These leaf traits might also explain in part why A per unit area varied about 5-fold in contrast to a 10-fold variation in A per unit mass among the species studied. Therefore, this might be an important point for explaining the relatively lower Apot as expressed on a mass basis of tree species.

In conclusion, the results suggest that regardless of the basis used for expressing Apot, the instantaneous potential photosynthetic rates for carbon fixation were similar among a variety of C3 and C4 tropical crop species studied here. Of course, the similarity in Apot values within these species was accounted for only by pre-existing components of the photosynthetic apparatus, as other attributes, such as enzyme amounts, would hardly have changed after short-term exposure (5-10 min) of leaves to saturating CO2. In any case, the similar values of Apot might have resulted from a conservative potential to fix CO2. Hence, the large differences in A observed here should be attributed to differential limitations to the overall photosynthetic process, and not to the photosynthetic capacity per se.



The authors are indebted to the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil) for fellowships and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) for financial support provided to their research projects. Many thanks are due also to Dr. Ernesto Medina for his critical reading of the manuscript and helpful comments.



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Received: 14/11/2000 -  Accepted: 3/4/2001
1. Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36571-000 Viçosa, MG, Brasil.
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