Carbon fixation via the CAM photosynthetic pathway

Three main types of photosynthetic pathway exist in higher plants. In the C3 type, the most widely distributed, CO2 fixation catalysed by the enzyme ribulosebisphos-phate carboxylase/oxygenase (Rubisco) results in the synthesis of a three-carbon acid. In C4 plants - for crops, mainly Graminaceae of tropical origin - CO2 is initially fixed by the enzyme phospho-enolpyruvate carboxylase (PEP-Case) into a four-carbon acid in leaf mesophyll cells. The four-carbon acid is then transported to adjacent bundle-sheath cells where decarboxyla-tion liberates CO2, which is fixed by Rubisco. This decarboxylation is accompanied by an increase in the intracellular CO2 concentration, which stimulates photosynthesis by inhibiting photorespiration and increases water-use efficiency (WUE) (Hatch, 1975; Wong et al., 1979). A third category of plants, which includes pineapple, also fix CO2 via PEP-Case and Rubisco. However, in these plants, a temporal separation occurs between the two carboxylation steps. Nocturnal fixation of CO2 occurs via PEP-Case, and the C4 acids synthesized, mainly malic, are stored in the vacuole. The following day, decarboxylation of malate liberates CO2, which is fixed by Rubisco. This type of photosynthesis, which results in large daily variations in the concentration of malate and which is found in species of the Crassulaceae, is termed crassulacean acid metabolism (CAM). The main feature of CAM plants is their high WUE. Mala te decarboxylation during the day is associated with an increase in the internal CO2 concentration and a subsequent decrease in the stomatal conductance, which reduces external CO2 uptake and transpiration (for reviews, see Kluge and Ting, 1978; Osmond, 1978; Winter, 1985). Pineapple is the most important crop species exhibiting CAM.

Photosynthetic rhythm in CAM plants and in pineapple

Rhythmic patterns of net CO2 exchange are well known in CAM plants, while photosyn-thetic O2 evolution is less well documented. The diel rhythm of CO2 fixation and O2 evolution of an attached pineapple 'D' leaf (Fig. 5.1) displays the typical four-phase pattern of net CO2 exchange in CAM plants described by Osmond (1978).

• Phase I corresponds to nocturnal carboxy-lation of phosphoenolpyruvate (PEP) via PEP-Case to form oxaloacetate (OAA). OAA is reduced to malate and stored in the chlorenchyma cell vacuoles. The internal CO2 partial pressure remains low during this time and stomatal conductance is high. The substrate for PEP production in pineapple is mainly soluble sugars (Borland and Griffiths, 1989; Carnal and Black, 1989). In terms of balance, internal CO2 from respiration is also fixed via PEP-Case and contributes to the malate pool. Night O2 uptake data (Fig. 5.1) indicate that, in a 'D' leaf, CO2 produced by respiration represents approximately 10% of the total CO2 fixed into malate at night (Côte, 1988). Night net CO2 fixation in pineapple generally accounts for at least two-thirds of the total net fixation of the day-night period (Neales et al., 1980; Bartholomew, 1982; Nose et al., 1986; Côte, 1988). Reported values for 21 studies in controlled environments with various photo- and thermoperiods and light levels ranged from 40 to 100%, with a mean of 80 ± 17% (Bartholomew and Malézieux, 1994). The proportion of CO2 fixed nocturnally by pineapple plants propagated in vitro shifted progressively from 0 to 70% as plant fresh weight increased from 1 to 300 g (Côte et al., 1993). These observations support the idea that pineapple is an obligate CAM plant.

• Phase II, at the beginning of the day, corresponds to the transition from net CO2 fixation via PEP-Case to CO2 fixation via Rubisco. Malate decarboxylation begins during this phase, the internal CO2 partial pressure gradually increases and stomatal

Photosynthesis Pineapple

Fig. 5.1. Net CO2 and O2 exchange rates of an attached 'Smooth Cayenne' pineapple 'D' leaf throughout a night/day cycle (Côte, 1988). Both CO2 fixation and O2 evolution are indicated as positive values. Positive values for O2 evolution during the day result from photosynthesis, while negative values during the night indicate O2 uptake due to respiration. The four phases of the CAM cycle as defined by Osmond (1978) are indicated at the top of the figure. Environmental conditions include: photosynthetic photon flux density, 400 ^mol m-2 s-1; photoperiod, 12 h night/12 h day; night/day temperature 22°C/26°C. Data are the average for 4 consecutive days.

Fig. 5.1. Net CO2 and O2 exchange rates of an attached 'Smooth Cayenne' pineapple 'D' leaf throughout a night/day cycle (Côte, 1988). Both CO2 fixation and O2 evolution are indicated as positive values. Positive values for O2 evolution during the day result from photosynthesis, while negative values during the night indicate O2 uptake due to respiration. The four phases of the CAM cycle as defined by Osmond (1978) are indicated at the top of the figure. Environmental conditions include: photosynthetic photon flux density, 400 ^mol m-2 s-1; photoperiod, 12 h night/12 h day; night/day temperature 22°C/26°C. Data are the average for 4 consecutive days.

conductance declines. The overall contribution to carbon gain is small during phase II and was 1-3% of the total day-night net CO2 uptake by pineapple plants maintained in controlled conditions (Fig. 5.1).

Phase III is a period when net CO2 fixation is negligible for up to 5 h, while CO2 generated by malate decarboxylation is fixed via Rubisco. The internal CO2 partial pressure rises well above atmospheric levels, because the rate of malate decar-boxylation exceeds the rate of internal CO2 fixation via Rubisco. Net CO2 release sometimes occurs during phase III. This high internal CO2 partial pressure stimulates photosynthesis and results in the low stomatal conductance, which limits transpiration during this phase. Although net CO2 uptake is nil during phase III, the maximum rate of photosynthetic carbon reduction via Rubisco occurs during this phase. Based on the assumption that 1.0 mol O2 is evolved for every mol CO2 reduced (Kaplan and Bjorkman, 1980), the rate of CO2 fixation via Rubisco during phase III, deduced from the rate of O2

evolution during this phase, could be 1.3-to six-fold higher than the maximum rate of net CO2 fixation achieved by pineapple during the light period (Côte, 1988). In the data of Fig. 5.1, it is 2.4 times higher. Phase IV begins when the malate pool becomes depleted, the internal CO2 partial pressure declines, stomatal conductance increases and net external CO2 uptake resumes for the last hours of the day. In pineapple, this fixation generally amounts to 15-25% of the total net CO2 uptake (Fig. 5.1). Early in the phase, there is a progressive shift from fixation of internally generated CO2 towards external net CO2 uptake. Following the assumption that 1.0 mol O2 is evolved per mole of CO2 fixed, it was estimated that only 60-80% of the total CO2 fixed during the night by a pineapple plant was reas-similated via Rubisco when net CO2 uptake resumed in phase IV (Côte et al., 1989). A value of 75% can be deduced from Fig. 5.1. PEP-Case has been reported to be active during late phase IV in CAM plants (Kluge, 1969; Kluge et al, 1982) and measurement of malate concentration also suggested that CO2 uptake via PEP-Case occurs in pineapple during late phase IV (Black et al., 1982; Kenyon et al., 1985). The O2 and CO2 gas-exchange data suggest that CO2 fixation via PEP-Case during phase IV represents 3-15% of the nocturnal net CO2 fixed by pineapple (Côte, 1988; Côte et al, 1989).

Gas exchange measured under controlled conditions (Fig. 5.2) is atypical of what occurs in the field, where stochastic, rather than steady-state, environmental conditions prevail. Diurnal changes in weather probably influence to some extent both the duration and the intensity of the four phases of CAM. While extrapolation of results obtained in controlled conditions to plants in natural environments must be done carefully, in situ measurement of stomatal conductance and leaf titratable acidity confirm the general conclusions derived from studies in controlled environments.

Photosynthetic rate in pineapple

In CAM plants, both net CO2 uptake and malate-decarboxylation-dependent CO2 assimilation via Rubisco during phase III have to be considered to evaluate the photo-synthetic rate. Net CO2 fixation in the light (phase IV) ranged from 0.13 to 6.3 ^mol m-2 s-1 for pineapple plants or 'D' leaves maintained in various conditions (Connelly, 1972; Neales et al., 1980; Sale and Neales, 1980; Côte, 1988; Bartholomew and Malézieux, 1994). Night net CO2-fixation values reported by the same authors ranged from 0.13 to 2.5 ^mol m-2 s-1, while others reported values as high as 5.0 to 7.8 ^mol m-2 s-1 (Côte, 1988; Borland and Griffiths, 1989; Fig 5.1). It can be deduced from photosynthetic O2 evolution that CO2 reduction via Rubisco never achieves a steady state in pineapple (Côte, 1988; Côte et al., 1989; Fig. 5.1). Data for O2 evolution from a pineapple 'D' leaf also show that the CO2 assimilation rate during

Obligate Cam Plants

Fig. 5.2. Controlled-environment chambers used for gas-exchange measurements of 'Smooth Cayenne' pineapple plants from in vitro culture (Côte, 1988). Measurements were made in controlled atmosphere automatic growth chambers (CEA, Commissariat à l'Energie Atomique, 13108 St Paul-lez-Durance, France).

Fig. 5.2. Controlled-environment chambers used for gas-exchange measurements of 'Smooth Cayenne' pineapple plants from in vitro culture (Côte, 1988). Measurements were made in controlled atmosphere automatic growth chambers (CEA, Commissariat à l'Energie Atomique, 13108 St Paul-lez-Durance, France).

phase III reaches 9.9 ^mol m-2 s-1, a value much greater than the maximum value observed in phase IV (Côte, 1988) (Fig. 5.1).

The maximum CO2-fixation rates for pineapple are comparable to those for other CAM plants, but are low compared with values of 8.33-25 ^mol m-2 s-1 reported for C3 plants (Black, 1973). The low rates for pineapple relative to those of C3 plants is in part due to low leaf conductances to gas diffusion during phase IV (Côte, 1988), even when the stomata are wide open. The concentration of Rubisco per unit area of leaf could also be low relative to C3 plants (Winter et al., 1982).

When CO2 fixation by pineapple is expressed on a unit area of soil, fixation rates are also much lower than those for C3 plants. For example, in controlled conditions, a pineapple plant with a leaf area index (LAI) close to 4 fixed 20-25% of the CO2 fixed by wheat (Côte et al., 1993). However, dry-matter accumulation by a pineapple crop is high. Lacoeuilhe (1976) reported that pineapple accumulated 41 t of dry matter ha-1 during a crop cycle in Côte d'Ivoire. Bartholomew (1982) reported 62 t of dry matter ha-1 in 24 months in Hawaii. By way of comparison, dry-matter production of wheat was reported to be between 18 and 29 t ha-1 year-1 (growing season), while that for sugar cane was 67 t ha-1 year-1 (Loomis and Gerakis, 1975). The large dry-matter accumulation by pineapple is associated with a high LAI and the ability of leaves to maintain their photo-synthetic capacity for long periods of time.

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