Article

The response of the C3-CAM tree, Clusia rosea, to light and water stress: I. Gas exchange characteristics

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Abstract

Gas exchange measurements were undertaken on 2-year-old plants of Clusia rosea. The plants were shown to have the ability to switch from C3-photosynthesis to CAM and vice versa regardless of leaf age and, under some conditions, CO2 was taken up continuously, throughout the day and night. The light response was saturated by 120 μmol m−2 s−1 typical of a shade plant. Gas exchange patterns in response to light, water and VPD were examined. All combinations of daytime and night-time CO2 uptake were observed, with rates of CO2 uptake ranging from 2 to 11 μmol m−2 s−1 depending upon water status and light. Categorization of this plant asC3, CAM or an intermediate is impossible. Differing VPD affected the magnitude of changes from CAM to C3-photosynthesis (0 to 0.5 and 0 to 6.0 μmol m−2 s−1 CO2, respectively) when plants were watered. Under well-watered conditions, but not under water stress, high PPFD elicited changes from CAM to C3 gas exchange. This is unusual not only for a shade plant but also for a plant with CAM. It is of ecological importance for C. rosea, which may spend the early years of its life as an epiphyte or in the forest understorey, to be able to maximize photosynthesis with minimal water loss.

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... The gas exchange patterns and organic acid accumulation was then studied in response to the light manipulations as a reliable way to monitor the CAM induction. Schmitt et al. showed in a rewatering experiment that C. minor is able to perform CAM in one leaf and C 3 -photosynthesis in the opposite leaf of the same leaf pair (Schmitt et al., 1988). This encouraged the use of one leaf as a control where the leaf was switched from C 3 -photosynthesis to CAM using high light conditions, while the opposite leaf was tested by selecting wavelengths and monitoring leaf responsiveness with respect to CAM induction. ...
... Most of the Clusia species studied so far are facultative CAM plants, in which CAM is induced by various environmental factors like drought, increased daytime temperature or increased irradiance (Grams et al., 1998;Lü ttge, 1999). CAM induction caused by high irradiance is well known and has been studied intensively, especially in C. minor (Schmitt et al., 1988;Franco et al., 1991;Haag-Kerwer et al., 1992;Borland et al., 1993Borland et al., , 1996Roberts et al., 1998;Herzog et al., 1999). It is shown here that the photoreceptor responsible for the CAM Table 1). ...
... On the other hand the values for ')400' and ')455' (2479 and 1392 mW m À2 , respectively) are above the threshold, since CAM was still induced by these wavelengths. Despite the fact that a threshold value for the CAM induction has to be reached, the C 3 uCAM transition might be a gradual process rather than an all-or-none response, since the amount of nocturnally fixed CO 2 is known to saturate with the integrated light sum from the previous day (Schmitt et al., 1988). The fact that CAM induction does not occur in experiments with wavelengths higher than 530 nm, shows that the maximum of the action spectrum for CAM induction is in the range of blue light. ...
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The high light‐induced switch in Clusia minor from C 3 ‐photosynthesis to Crassulacean acid metabolism (CAM) is fast (within a few days) and reversible. Although this C 3 /CAM transition has been studied intensively, the nature of the photoreceptor at the beginning of the CAM‐induction signal chain is still unknown. Using optical filters that only transmit selected wavelengths, the CAM light induction of single leaves was tested. As controls the opposite leaf of the same leaf pair was studied in which CAM was induced by high unfiltered radiation ( c . 2100 μmol m ⁻² s ⁻¹ ). To evaluate the C 3 ‐photosynthesis/CAM transition, nocturnal CO 2 uptake, daytime stomatal closure and organic acid levels were monitored. Light at wavelengths longer than 530 nm was not effective for the induction of the C 3 /CAM switch in C. minor . In this case CAM was present in the control leaf while the opposite leaf continued performing C 3 ‐photosynthesis, indicating that CAM induction triggered by high light conditions is wavelength‐dependent and a leaf internal process. Leaves subjected to wavelengths in the range of 345–530 nm performed nocturnal CO 2 uptake, (partial) stomatal closure during the day (CAM‐phase III), and decarboxylation of citric acid within the first 2 d after the switch to high light conditions. Based on these experiments and evidence from the literature, it is suggested that a UV‐A/blue light receptor mediates the light‐induced C 3 ‐photosynthesis/CAM switch in C. minor .
... Plants of C. minor are evergreen small freestanding trees, hemi-epiphytes or strangler holo-epiphytes; they live in a broad range of environments, from forests to savannas, and from the forest floor to tree branches (Lüttge 2006). In C. minor CO 2 fixation is best characterised as C 3 -CAM; watered plants of C. minor show nil nocturnal acid accumulation (DH + ), while a short period of drought is capable of inducing the appearance of nocturnal CO 2 fixation with concomitantly high values of DH + (Schmitt et al. 1988). CAM is extremely plastic in this species; in one single branch, leaves subjected to drier air performed CAM, whereas the opposite leaves, under humid air, did not (Schmitt et al. 1988). ...
... In C. minor CO 2 fixation is best characterised as C 3 -CAM; watered plants of C. minor show nil nocturnal acid accumulation (DH + ), while a short period of drought is capable of inducing the appearance of nocturnal CO 2 fixation with concomitantly high values of DH + (Schmitt et al. 1988). CAM is extremely plastic in this species; in one single branch, leaves subjected to drier air performed CAM, whereas the opposite leaves, under humid air, did not (Schmitt et al. 1988). The shift between C 3 photosynthesis and CAM is rapid and plastic under both field and controlled conditions (Borland et al. 1996; Haag-Kerwer et al. 1996; Schmitt et al. 1988; Mattos et al. 1999 water potential (w), leaf osmotic potential (w s ) and turgor potential (w T ) was small and little influenced by water availability or evaporative demand; DH + was high under mild drought and nil after prolonged drought or rains (Zotz and Winter 1994). ...
... CAM is extremely plastic in this species; in one single branch, leaves subjected to drier air performed CAM, whereas the opposite leaves, under humid air, did not (Schmitt et al. 1988). The shift between C 3 photosynthesis and CAM is rapid and plastic under both field and controlled conditions (Borland et al. 1996; Haag-Kerwer et al. 1996; Schmitt et al. 1988; Mattos et al. 1999 water potential (w), leaf osmotic potential (w s ) and turgor potential (w T ) was small and little influenced by water availability or evaporative demand; DH + was high under mild drought and nil after prolonged drought or rains (Zotz and Winter 1994). It is currently accepted that CAM is an adaptation to dry environments that helps the plant attain higher water use efficiency than C 3 or C 4 plants (Winter 1985). ...
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Clusia minor L. is a C3-CAM species in which Crassulacean acid Metabolism (CAM) is induced, among other factors, by water deficit. We propose that CAM induction by natural drought in C. minor shifts the sap flow pattern from daytime to a night-time one, and that the decreased osmotic potential due to increased malate content in droughted plants aids in the increase in nocturnal sap flow. In order to test these hypotheses, we followed for 2 years the seasonal changes in parameters of water relationships and sap flow velocity in one single, freestanding tree growing in Caracas. Leaf water and osmotic potential were measured psychrometrically, nocturnal proton accumulation by titration of aqueous leaf extracts and sap flow density with thermal dissipation probes. Leaf water, osmotic and turgor potential remained relatively high throughout the seasons. Nocturnal proton accumulation was nil under extreme drought or after frequent and heavy rains, and high after moderate rainfall. Estimated malate and citrate concentrations contributed up to 80 and 60%, respectively, of the value of osmotic potential. The shape of the daily courses of sap flow velocity varied seasonally, from mostly diurnal during the dry season to mostly nocturnal after a short dry spell during the rainy season, when nocturnal acid accumulation attained high values. There was a strong positive relationship between the proportion of the integrated sap flow courses corresponding to the night and dawn [H+] (r 2 = 0.88). Increased nocturnal sap flow in the CAM stage of the tree of C. minor may be explained by a lower osmotic potential due to an increased acid concentration, together with increased stomatal aperture, as suggested by increased nocturnal acid accumulation probably due to nocturnal CO2 fixation.
... Moreover, some species within the genus Clusia show an enormous flexibility in switching fronn C3 photosynthesis to CAM and vice versa in response to changes in environmental conditions. This was not only shown under laboratory conditions (Franco, Ball & Luttge, 1990, 1991Haag-Kerwer, Franco & Luttge, 1992;Schmitt, Lee & Luttge, 1988;Winter et al., 1992) but also in the field (Borland et al., 1993;Franco et al., 1994;Zotz & Winter, 1993). An annual shift between Cg photosynthesis and CAM was described by Borland et al. (1992) and Zotz & Winter (1994), who found night-time CO, uptake during the dry season while gas-exchange patterns typical for Cg photosynthesis were only found during the wet season. ...
... Characteristic of many Clusia species is the ability to accumulate enormous amounts of malate and citrate during the night (Popp et al., 1987;Franco et al., 1990). Although it is well established that nighttime malate accumulation in CAM plants serves as primary storage of COg gathered from the atmosphere, this is not true for citrate accumulation (Luttge, 1988). Carbon dioxide internally released by respiration can be refixed into malate (Griffiths, 1988), which can then be converted to citrate in the mitochondria (Olivares et al., 1993). ...
... Whether decarboxylation of malate and citrate during phase III of CAM affects photosynthetic light-use efficiency can be assessed by comparing the potential rates of CO2 release from organic acids with apparent electon transport rates at PS II (Fig. 6). The CO2 potentially available for photosynthetic CO2 fixation via Rubisco, when stomata are almost closed during the light period in CAM, can be calculated from the breakdown of organic acids, where each malate molecule gives one molecule of COg, whereas each citrate molecule can give either one or three molecules of COg depending on whether it is broken down to a-oxoglutarate or pyruvate (Haag-Kerwer et al., 1992;Luttge, 1988). Although our field data were highly variable, a significant correlation between decarboxylation rate and apparent ETR was found for C. rosea, assuming the generation of one mole of COg per mole of citrate decarboxylated (r = 0-93, p = 0-05), but for Clusia sp. ...
Article
summaryFour different Clusia species showing C3 photosynthesis (C. multiflora) or crassulacean acid metabolism (CAM) (C. rosea, an unidentified Clusia sp. and C. alata) co-occur in the same habitat in the northwest of Venezuela. The aim of this field study was to correlate the adaptive changes in chlorophyll a fluorescence with gas exchange patterns and deacidification of nocturnally accumulated organic acids.The results indicate that in C. rosea and Clusia sp. a lowering of the potential quantum yield, measured as Fv/Fm after 10 min of dark adaptation, is restricted to the early morning hours. With the onset of deacidification there was no further decline in Fv/Fm, although the irradiance upon the leaves remained high. For the C3-plant, C. multiflora, changes in Fv/Fm were correlated with changes in irradiance incident on the leaves before predarkening for 10 min for Fv/Fm measurements. The fast relaxation of Fv/Fm under low light indicates that C. multiflora was not suffering photoinhibitory damage. Effective quantum yield as determined by ΔF/Fm, was low under high irradiances for C. rosea and Clusia sp. and did not change significantly for C. rosea during phase III of CAM. During the time of low incident irradiance C. alata and C. multiflora reached an effective quantum yield that was close to the optimal quantum yield of electron transport. It is noteworthy that apparent electron transport rates through photosystem II (PS II) (ΔF/F'm) × PPFD) were highest for C. rosea, Clusia sp. and C. alata during phase III of CAM. Electron transport rates in C. multiflora were lower under high irradiance and did not differ from those found in phases II and IV of CAM. The possible role of CO2, evolution from acid decarboxylation with respect to photosynthetic efficiency is discussed.
... Ce type de plante a inspiré de nombreux travaux. Bessey (1908), Richards ( 1952) et Rami rez ( 1977 se sont intéressés à leur aptitude à germer sur un support où l'implantation est a priori problématique. Richards (1952), Madison (1977), Putz & Holbrook ( 1986) ont étudié les structures morphologiques et anatomiques des tiges et des feuilles, permettant à ces plantes de ré sister au stress hydrique causé par leur exposition au soleil. ...
... Bessey (1908), Richards ( 1952) et Rami rez ( 1977 se sont intéressés à leur aptitude à germer sur un support où l'implantation est a priori problématique. Richards (1952), Madison (1977), Putz & Holbrook ( 1986) ont étudié les structures morphologiques et anatomiques des tiges et des feuilles, permettant à ces plantes de ré sister au stress hydrique causé par leur exposition au soleil. Ils ont mis aussi en évidence l'existence de plusieurs types anatomiques et fonctionnels de racines qui permettent l'ancrage ou la nutrition de l'organisme. ...
... At the beginning of the dry season, exposed plants showed continuous uptake of CO.^ over 24 h albeit with reduced rates of photosynthesis over the middle part of the day. Similar results have been shown in the laboratory for this and a number of other Cg-CAM intermediates (Schmitt et al, 1988;Griffiths, 1989;Franco et al, 1991). ...
... However, rates of net dark uptake of COg were substantially lower than other reported rates for this species in both the field and the laboratory (Ting et al, 1987;Schmitt et al, 1988) and night-time fixation accounted for only a small proportion of COj fixed over 24 h. ...
Article
SUMMARYA study was made of photosynthesis and expression of crassulacean acid metabolism (CAM) in naturally exposed and shaded populations of Clusia minor L. during the transition from wet to dry season in Trinidad (mid-February to mid-April, 1990). At the start of the dry season, plants from exposed and shaded habitats showed a capacity for CAM either through the fixation of external or internal (respiratory) CO2. Exposed plants showed continuous uptake of CO2 over 24 h although dark fixation accounted for only a small proportion of CO2 fixed over the day. The expression of CAM was considerably enhanced as the dry season progressed with substantial increases in the overnight accumulation of titratable acidity, particularly in leaves of exposed plants. This was accompanied by a reduction in day-time photosynthesis and an increase in dark fixation, with shaded plants showing only night-time fixation of CO2. The magnitude of CAM in C. minor was substantial with a maximum ΔH+ of 1410 mol m-3 measured in leaves from exposed branches. Both malic and citric acids were accumulated overnight. The highest citric:malic acid ratios were found in young leaves from exposed plants with 250 mol m-3 malic and 125 mol m-3 citric acid accumulated near the time of maximum CAM activity. Photosynthetic efficiency, measured as light responses of O2 evolution, also varied on a daily basis dependent on the incident photosynthetic photon flux density (PPFD). Apparent quantum yield and photosynthetic capacity showed marked reductions depending on the degree of exposure, suggesting that photoinhibitory responses are important under natural conditions. An analysis of three members of the Clusiaceae endemic to Trinidad showed that each had the capacity to induce CAM activity, despite being found in a narrow range of habitats which have higher rainfall than those of C. minor. However, despite the variable expression of CAM activity, carbon isotope composition suggested that when integrated throughout the year, carbon accumulation is predominantly mediated via the C3 pathway in all the species studied.
... This sofar has been found to be the most versatile CAM plant (see Introduction). Leaves of well watered plants tend to change their metabolism from a CAM-like pattern to a more C 3 -like behaviour when transferred from low light to high light (Schmitt et al., 1988). Thus, when water is not limiting and stomatal opening can be afforded, effective C 3photosynthesis during the day appears to be the best approach to prevent photoinhibition at high light conditions and then nitrogen-use-efficiency may also increase (Figs. 5 and 6). ...
Article
Plants of Kalanchoe pinnata (Lam.) Pers. were grown in the glass chamber of a phytotron in high-light (16-23 mol photons m-2 day-1) and in the shade (0.8-2.1 mol photons m-2 day-1) respectively, without or with nitrogen nutrition (12 mol m-3 NO3- in irrigation solution) and well watered or droughted for 18-22 days (high-light) and 26 to 32 days (shade) respectively, prior to measurements and analyses. Part of the high-light plants were transferred to the shade and part of the shade plants to high-light before measurements. Gas-exchange (H2O-vapour, CO2) was measured and contents of total leaf nitrogen, chlorophyll a and b and carotenoids were analysed. Both high-light and low-light grown plants showed typical CAM gas exchange. When high-light plants were transferred to the shade under all conditions diurnal net CO2-balance was negative. Shade plants transferred to high-light greatly increased their daily net CO2-uptake, particularly by extended CO2-fixation at high rates in the light period, if supplied with H2O and N. Thus, shade plants were very successful in high-light provided N and H2O were not limiting. Shade adaptation of shade-plants as compared to high-light plants was indicated by higher absolute chlorophyll and carotenoid contents and lower chlorophyll a/b as well as lower CO2-uptake to chlorophyll (a + b) ratios. The results show, that the factors irradiance, nitrogen-nutrition and water-availability interact in eliciting flexible responses of the photosynthetic mechanism in the constitutive CAM-plant K. pinnata. Highlight plants were not shade tolerant; low-light plants were shade tolerant but not shade demanding.
... Leaf-to-air vapour pressure difference (VPD) has been inferred to play a major role in the photosynthetic pathway control of Clusia minor. Schmitt et al. (1988) showed that, following rewatering of water-stressed CAM-performing Clusia minor, the reversion to C 3 photosynthesis occurred more rapidly when VPD was low (6.2 vs 13.1 mbar). This experiment has been erroneously interpreted to suggest that high VPD can rapidly induce CAM (Dodd et al., 2002;Matiz et al., 2013). ...
Article
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Facultative crassulacean acid metabolism (CAM) describes the optional use of CAM photosynthesis, typically under conditions of drought stress, in plants that otherwise employ C3 or C4 photosynthesis. In its cleanest form, the upregulation of CAM is fully reversible upon removal of stress. Reversibility distinguishes facultative CAM from ontogenetically programmed unidirectional C3-to-CAM shifts inherent in constitutive CAM plants. Using mainly measurements of 24h CO2 exchange, defining features of facultative CAM are highlighted in five terrestrial species, Clusia pratensis, Calandrinia polyandra, Mesembryanthemum crystallinum, Portulaca oleracea and Talinum triangulare. For these, we provide detailed chronologies of the shifts between photosynthetic modes and comment on their usefulness as experimental systems. Photosynthetic flexibility is also reviewed in an aquatic CAM plant, Isoetes howellii. Through comparisons of C3 and CAM states in facultative CAM species, many fundamental biochemical principles of the CAM pathway have been uncovered. Facultative CAM species will be of even greater relevance now that new sequencing technologies facilitate the mapping of genomes and tracking of the expression patterns of multiple genes. These technologies and facultative CAM systems, when joined, are expected to contribute in a major way towards our goal of understanding the essence of CAM.
... Diversity of CAM inducibilty is marked within the genus Clusia[159][160][161]. In Clusia minor, opposite leaves on the same node are capable of expressing either C 3 or full CAM characteristics, depending on the leaf–air vapor pressure difference[162], whereas in Clusia uvitana, rapid and reversible switching between C 3 photosynthesis and CAM can occur within 24 h in response to environmental changes[163]. Spatial separation of CAM inducibility is found in Cissus quadrangularis, a species with succulent CAM stem bearing small, short lived leaves that can switch from CAM cycling to CAM under conditions of moderate stress[164]. ...
... In addition, the accumulation in leaf titratable acidity for CAM plants was observed in plants under well-watered growth chamber conditions (Table 1). In facultative species, CAM may be induced by environmental factors such as high PPF (Maxwell, 2002), temperature (Haag-Kerwer et al., 1992), and the relative air humidity (Schmitt et al., 1988). The dark net CO 2 exchange percentages of the 2 d in the Beijing greenhouse were 10.7 and 12.2 times that in the growth chamber. ...
Article
Dendrobium officinale, endemic to China, is a rare and endangered medicinal herb. As a result of its high economic value, slow growth, and diminishing wild population, protected cultivation is preferred. However, little information is available on its growing environment and photosynthetic characteristics. In this study, the photosynthetic patterns of D. officinale were investigated under various environmental conditions by measuring the net CO2 exchange rates continuously for several days or weeks. Under non-stressed growth chamber conditions with 12-hour light and 12-hour dark periods, D. officinale had concomitance of C3 and crassulacean acid metabolism (CAM) photosynthesis patterns. Different degrees of CAM in D. officinale, expressed as the percentage of CO2 exchanges in the dark period to the daily amount of CO2 exchanges, were observed depending on environmental conditions. With decreasing substrate water content, a typical CAM pattern was found, and concomitance of C3 and CAMpatterns was found again when plants were rewatered. The accumulation of leaf titratable acidity during a dark period increased as substrate dried out but decreased again as plants were rewatered. A shorter light-dark cycle (4-hour light and 4-hour dark periods) led to a C3 pattern alone. The substrate moisture and light-dark cycle were inducible factors for switching between C3 and CAM patterns in D. officinale. These results indicate that D. officinale is a facultative CAM plant and the C3 pathway can be induced by controlling the growing environment. Further studies are needed to identify the optimal environmental conditions to enhance the growth of D. officinale.
... For example, in outer-canopy leaves at tbe Ceiba site, the relative contribution of net dark CO2 fixation to 24-h carbon gain w-as tnuch lower (about 13",,) during most parts of the wet season (May-September; Period 2), w-hen C. uvitana was shaded by the leaves of its host tree tban during the last tw-o months of the wet season, when shading did not occur (Period 3). in absolute terms, nocturnal carbon gain was e\'en higher than during the dry period w'ith shading (Period 1). Tbe increased CAM activity in C. uvitana under conditions of increased PPFR contrasts with results obtained in short-term laboratory studies witb well-watered Clusia minor, in which abrupt increases in PPFR led to the elimination of net dark CO^ fixation (Schmitt, Lee & Luttge, 1988). Part of tbe sbift to more pronounced nocturnal CO. uptake after the abscission of the host tree may have been related to decreased minimum temperatures. ...
Article
Diel (24 h) courses of CO2 and water-vapour exchange of leaves of hemi-epiphytic plants of Clusia uvitana Pittier (Clusiaceae) were measured under natural tropical conditions in the semi-evergreen moist forest of Barro Colorado Island, Panama, from January 1991 until January 1992. Plants were studied at two sites, in the crown of a 47-m tall tree (Ceiba pentandra) and on the shore of Lake Gatun, at a height of about 2–4 m. The following results were obtained: (1) Diel carbon gain was mainly a function of photosynthetic photon fluence rate (PPFR) on individual days. PPFR also strongly affected CAM activity. A leafless period of the host tree Ceiba pentandra resulted in higher incident PPFRs and slightly lower nighttime temperatures in the canopy of C uvitana; this led to increases in both daytime and nighttime CO2 fixation. (2) In fully mature sun leaves from the two sites, nocturnal net uptake of atmospheric CO2 occurred on almost all of the 71 days measured and nocturnal carbon gain was enhanced during the dry season. (3) In C. uvitana at the Lake site, 24-h carbon gain during the wet and dry season was similar to C. uvitana at the Ceiba site during the leafless period of the host tree. Overall CAM activity was lower at the Lake site. (4) Recycling of respiratory CO2 was a major route for nocturnal acid synthesis. Nocturnal net uptake of atmospheric CO2 was closely correlated with changes in titratable acidity, but accounted for only about 30% of the nocturnal increase in organic acids. (5) Mature shade leaves performed CAM only during the dry season, whereas in the wet season they showed atmospheric CO2 uptake exclusively in the light. (6) Independent of exposure or season, leaves less than about 12 wk old showed a C3 pattern of diel gas exchange and the level of titratable acidity was high day and night. (7) The annual carbon budget of outer canopy leaves of C uvitana in the Ceiba site was 1780 g CO2 m-2 a-1 and the average long-term water-use efficiency was 23 × 10-3 g CO2 g-1 H2O. (8) Vegetative growth was strongly seasonal. Branch length increment and leaf area development was much higher in the wet season. Mineral element contents in these evergreen plants showed no age-related changes, but a significant proportion of elements was retrieved before abscission.
... In addition, the accumulation in leaf titratable acidity for CAM plants was observed in plants under well-watered growth chamber conditions (Table 1). In facultative species, CAM may be induced by environmental factors such as high PPF (Maxwell, 2002), temperature (Haag-Kerwer et al., 1992), and the relative air humidity (Schmitt et al., 1988). The dark net CO 2 exchange percentages of the 2 d in the Beijing greenhouse were 10.7 and 12.2 times that in the growth chamber. ...
... In fact, the genus Clusia represents a magnificent example of diversity and inducibility of CAM. In Clusia minor, for example, opposite leaves on the same node can perform either C 3 or CAM in response to different temperatures and leaf-air vapor pressures, as only the leaves maintained in dry air conditions were capable of expressing CAM [26]. Among Clusia species, C. minor is currently the most widely used model for C 3 -CAM photosynthesis studies [18,20,27,28]. ...
... The C 3 pathway is utilised to maximise growth when water is abundant, while the C 3 -to-CAM transition reduces water loss under water deficit conditions, nevertheless, photosynthetic integrity is maintained that ultimately translates into reproductive success (Winter and Ziegler, 1992). It was observed that opposite leaves of Clusia minor, depending on the relative humidity of the air surrounding them, may or may not follow CAM (Schmitt et al., 1988), while the CO 2 exchange pattern of droughted plants of Talinum triangulare after re-watering reverted from idling to purely daytime assimilation (Herrera et al., 1991). ...
Chapter
Crassulacean acid metabolism (CAM)‐cycling plants display both the C3 and CAM photosynthetic pathways at various extents in response to environmental and plant physiological conditions. Evolved from the C3 metabolism, CAM is a photosynthetic adaptation specialised to improve plant water‐use efficiency by shifting/extending the CO2 uptake from the day to the night. Obligate CAM plants such as the Agave species, pineapples, orchids, and prickly pears are highly productive and respond favourably to extreme heat and drought, and water‐limited environments. In comparison to the C3 and C4 plants, agricultural CAM crops can thrive in semi‐arid and arid lands, making them an ideal and sustainable commercial crop for food and energy. Very few plants exhibit the CAM‐cycling pathway, while the fairly well‐known examples include Mesembryanthemum crystallinum (ice plant) and Jatropha curcas (physic nut). In such plants bestowed with the ability to interchange different photosynthetic metabolisms, little is known on how each unique photosynthetic metabolism is likely to contribute to overall plant growth and development. This article explores the utilisation of CAM for biomass and yield improvement in a bioenergy crop (J. curcas) conferred with CAM‐cycling photosynthetic machinery. The J. curcas photosynthetic‐associated parameters, yield components in relation to transcriptomic data analyses from previous studies are described and discussed to benefit plant breeding programs targeted for productivity enhancement.
... Gas exchange of Clusia CAM species has been shown to be highly flexible, going from typical CAM to typical C3, including continuous net fixation of CO 2 during a 24 h cycle, depending on light intensity during growth, day-night temperature cycles, drought, and even nutrition (Schmitt et al. 1988, Lee et al. 1989, Zotz and Winter 1993. Drought induces contrasting effects on Clusia species that fix CO 2 during the night. ...
Chapter
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The analysis of the functional properties of tropical forests components, and of the forest as a whole, continues to develop at a fast pace as a result of the international efforts to study the forest–atmosphere interactions within the context of global climate and land-use change. These efforts are directed to develop operative models capable of quantifying the role of tropical forests in the dynamics of trace greenhouse gases in the atmosphere. The discussion on the impact of increasing atmospheric CO2 concentrations on the productive performance of tropical forests goes on strongly. A number of groups maintain the notion that elevated CO2 concentrations in the atmosphere may be stimulating the photosynthetic capacity of tropical forests resulting from a ‘‘fertilization’’ effect. However, others maintain that these effects may be counteracted by water limitations (in water-limited systems) or by nutrient limitations as most humid tropical forests grow on substrates of limited fertility. Some recent developments show that tropical humid forests in the Amazon basin may be acting as a sink for CO2. In addition, there are already some promising modeling efforts integrating the physiological and ecological knowledge on the effects of CO2 on photosynthesis and the capability for nutrient uptake under natural conditions (Lloyd and Farquhar 1996). We can expect dramatic developments in the understanding of the physiological ecology of the production processes in tropical forests during the near future. This will be of utmost importance for future restoration efforts considering the rate of land-use change in the tropics.
... In contrast to always positive daily sap flow in the SE_stem, flow on the north-western stem side was often either zero or negative. We do not think however that this is a signal of CAM although different plant sides may possibly show signs of both types of photosynthesis (Schmitt et al. 1988). The reason for the frequent zero or negative flow in the NW_stem is rather the absence of direct axial connection with the roots. ...
Article
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Dracaena cinnabari is a relict of the remote Socotra Island (Yemen) where it grows at higher altitudes with the frequent occurrence of fogs. D. cinnabari as the only representative of the dragon tree group creates woodlands and forests on the Socotra Island. It is not clear what mechanisms allow this relict arborescent monocot to survive harsh climate and poor soil of karst rocks there. In this work, we conducted long-term sap flow monitoring in the stem and roots of the mature D. cinnabari plant during the driest period of year between two regular monsoons. We aimed to reveal plant responses to a range of environmental conditions and to understand mechanisms of drought survival by this woody monocot. Several following features of sap flow performance were found: high flow sectoriality in the stem and in roots corresponding to the intensity of insolation, free lateral flow, higher stem integrity compared to roots, internal storage replenishment from the fog followed by increased transpiration presumably from the refilled stem storage. Results indicate that in studying the sap flow dynamics in the mature D. cinnabari tree, plant water storage should be included in the analyses in addition to soil water availability and intensity of evaporating demands. The ability to replenish succulent woody organs from atmospheric water and to survive long periods of drought from the internal supply distinguishes the behavior of this short-rooted arborescent monocot from the known strategies of deep-rooted trees in arid areas.
Article
Guzmania monostachia (L.) Rusby ex Mez is an epiphytic, rosette-shaped bromeliad that displays variable degrees of crassulacean acid metabolism (CAM) along the leaf under water deficit. The aim of our study was to evaluate whether the production-scavenging system of reactive oxygen species (ROS) along the leaf length of G. monostachia plants is related to the foliar gradient of CAM when irrigation is withheld. Among the leaf portions, the apex was exposed to the highest photosynthetic flux density and presented the highest relative water content, CAM activity, hydrogen peroxide and lipid peroxidation after treatment. Hence, the most intense CAM at the leaf apex may not have prevented higher oxidative burden in that region during water deficiency. However, the photosynthetic efficiency in the apex seemed unaffected by irrigation withholding or light intensity. The leaf apex also had the highest carotenoid content and increased superoxide dismutase and ascorbate peroxidase activities under treatment. Hence, G. monostachia was able to maintain ROS under tolerable levels by increasing antioxidant capacity. Our results suggest the metabolic differences within the same leaf under water deficit may derive from the gradient of light incidence, which emphasises the physiological plasticity this bromeliad applies to adapt to the adverse conditions of the canopy.
Article
The content of the xanthophylls violaxanthin, antheraxanthin and zeaxanthin, which are interconvertible in the so-called xanthophyll cycle in the chloroplasts, was determined in leaves of the crassulacean-acid-metabolism plant, Clusia rosea, at the end of a 12-h dark period and at three times during a 12-h photoperiod of constant illumination (200 μmol photons·m(-2)·s(-1)). Whereas the level of violaxanthin was high at the end of the dark period and that of zeaxanthin low, zeaxanthin increased and violaxanthin decreased during the early light period, when atmospheric CO2 was taken up rapidly by the leaves. In the middle of the light period, when net uptake of atmospheric CO2 was not observed, yet when decarboxylation of malic acid allowed for high rates of CO2 reduction in the chloroplasts, zeaxanthin was low and violaxanthin was high. At the end of the light period, when uptake of atmospheric CO2 re-occurred, zeaxanthin increased again and violaxanthin decreased. Measurements of chlorophyll-a fluorescence with a modulated fluorometer showed that the increases in the level of zeaxanthin during the early and late light period were paralleled by decreased rates of electron transport and by increased rates of nonradiative dissipation of excitation energy.
Article
The importance of ontogeny and the degree of abiotic stress in determining the interplay between facilitation and competition is well known. However, their joint effect on the outcome of plant interactions remains poorly understood, especially when a continuous gradient of abiotic stress is considered. Our objective was to evaluate the frequency of association of individuals of Clusia criuva with typical coastal dune species across a gradient of water stress and how this association affects the growth of juveniles and sub-adults. The study was performed in a coastal dune region in South Brazil, where the sandy soil promotes severe water stress. One-year growth of 293 individuals and their distance to the closest humid slacks were measured. This distance is a good surrogate for water stress, since slacks represent proximity to groundwater. The proportion of associated individuals increased with abiotic stress in both ontogenetic stages, but was always greater for juveniles. This suggests that association is progressively more important to guarantee survival as abiotic stress increases. Nonetheless, the benefit of neighbors to growth decreased with abiotic stress, and associated plants grew less than isolated ones in harsher environments. This was mainly true for juveniles, since the height growth of sub-adults was not affected by association or abiotic stress. In our study, facilitation became more intense with environmental severity, increasing survival, although competition also became more influent, reducing growth particularly for younger plants. This demonstrates that ontogenetic stage and abiotic stress must be considered simultaneously in order to better understand interactions among plants.
Article
Most of the species in the genus Clusia are very flexible in their photosynthetic pathway, and are C3-photosynthesis/Crassulacean acid metabolism (CAM) intermediate species; therefore, the identification and clear assignment of Clusia-species to C3- or CAM-pathways is difficult. We made an attempt to characterize obligate C3-photosynthesis species within that genus. Therefore, we selected five species of the family Clusiacea (four of the genus Clusia and one of the genus Oedematopus) on the basis of their low leaf succulence as potential obligate C3-photosynthesis species. All of them showed a C3-photosynthesis pattern of gas exchange under well-watered conditions and their δ13C-values were also found to be in the range of obligate C3-photosynthesis plants. Under drought stress two of them (C. articulata and C. cruiva) proved to be C3-photosynthesis/CAM intermediate species, while C. parviflora, C. multiflora and most likely O. mirandensis did not show any nocturnal CO2-fixation. However, in C. parviflora and O. mirandensis some nighttime accumulation of malate by internal CO2-recycling might occur. So far, C. multiflora seems to be the only known Clusia species with neither nocturnal net CO2-uptake nor malate accumulation.
Article
Well-watered plants of Crassula sieberiana were shown to perform C3-type of photosynthesis independently of photoperiodic regimes. Abrupt drought conditions shifted the plants to CAM or CAM-like situations according to CO2-exchange patterns, levels and diel oscillation of malate pools and phosphoenolpyruvate carboxylase capacity (EC 4.1.1.31 PEPC). Progressively increased levels of drought under long days resulted, at each step, in reversible increase in PEPC extractable activity, independently of other CAM criteria (CO2 exchange patterns and diel oscillation of malate). Immunotitration experiments showed that the increase in PEPC was due to de novo synthesis of the enzyme. No correlation could be found between PEPC synthesis and water parameters of the leaves. The primary triggering element for the observed changes remains to be discovered.
Article
Sedum telephium is a C3/CAM intermediate plant in which expression of CAM is caused by water deficit. The timing of the C3-CAM switch and its relationship with water status and phosphoenolpyruvate (PEP) carboxylase activity have been investigated. Water deficit was provided by application of polyethylene glycol (PEG) solutions so that roots were exposed to water potentials from 0 to − 2.0 MPa below that of the nutrient solution. The response of the plants was measured during the first dark period after PEG addition and 7 d later. Malic acid accumulation was triggered during the first dark period at root water potentials of −0.3 MPa or less. This corresponded with very small decreases in leaf water potential and relative water content. The capacity of PEP carboxylase was not altered at any water potential during the first dark period. After 7 d the capacity of PEP carboxylase progressively increased as water potential declined to −0.4 MPa. At this, and more negative, water potentials it was 5-fold higher than in well-watered leaves. Malic acid fluctuations increased with decreasing PEG water potential below a threshold of −0.1 MPa. Malic acid levels at the end of the light period were progressively lower as water potential decreased. NAD- and NADP-malic enzyme activity were not affected by low water potential. Leaves detached from well-watered plants in the middle of the light period and kept hydrated did not accumulate malic acid during the following dark period. Allowing the leaves to lose 10% of their water content induced malic acid accumulation during the same time. Conversely, leaves detached from long-term droughted plants (which had malate fluctuations and a PEP carboxylase capacity 5-fold higher than well-watered plants) accumulated malate during the night if maintained at the same low hydration state (82%RWC), whereas malic acid accumulation was promptly reduced if they were rehydrated. Malic acid accumulation could therefore be rapidly altered by changing the hydration state of the leaves. The short-term rehydration treatments did not alter PEP carboxylase capacity. However, alteration of leaf hydration affected the apparent Km (PEP) of PEP carboxylase extracted 1 h before the end of the dark period. The Km was increased by rehydration and decreased by dehydration. Sensitivity to feedback inhibition by malate was not affected by hydration state and was high for PEP carboxylase from well-watered leaves and lower for PEP carboxylase from long-term droughted leaves. Taken together, the responses of intact plants and detached leaves show that malic acid accumulation can be triggered very rapidly by small water deficits in the leaves. The extent of night-time malic acid accumulation is independent of PEP carboxylase capacity. However, a change in the hydration state of the leaves can rapidly alter the affinity of PEP carboxylase for PEP. The regulation of malic acid accumulation in relation to the drought-induced triggering of CAM is discussed.
Article
For the first time the expression of C3 and CAM in the leaves of different age of Marrubium frivaldszkyanum Boiss, is reported. With increasing leaf age a typical C3 photosynthesis pattern and high transpiration rate were found. In older leaves a shift to CAM occurred and the 24-h transpiration water loss decreased. A correlation was established between leaf area and accumulation of malate. Water loss at early stages of leaf expansion may be connected with the shift to CAM and the water economy of the whole plant.
Article
Conditions and maintenance of growth were chosen so that plants of Clusia minor L. were obtained which showed the C3- and CAM- modes of CO2-exchange, respectively. C. minor is known to accumulate considerable amounts of citric acid in addition to malic acid during the dark-phase of CAM. ¹⁴CO2-pulse-chase experiments were performed with these plants. Patterns of labelling during the pulse and redistribution of label during the chase in the C3-mode were as expected for C3-photosynthesis. Pulse-labelling in the CAM-mode during the last hour of the light period, during the first part of the dark period and during the last hour of the dark period always led to an almost exclusive incorporation of label into malate. Redistribution of label from malate after the pulse at the end of the dark period during the chase in the subsequent light period followed the pattern expected for light-dependent reassimilation of CO2 remobilized from malate in CAM during the light period. During the chases in the dark period, label was transferred from l4C-malate to citrate. This suggests that during accumulation of citric acid in the dark period of CAM in C. minor, citrate is synthesized in the mitochondria from malate or oxaloacetate after formation of malate via phosphoenolpyruvate carboxylase. The experiment also showed that no labelled compounds are exported from leaves in the CAM-mode during the dark period. In plants of the C3-mode the roots proved to be strong sinks.
Article
CO2 gas exchange and nocturnal acidification was studied in situ and in the laboratory on 7 woody hemiepiphytes representing 6 genera in 4 families. CAM activity was detected only in the genus Clusia, but a species of another genus in the same family (Havetiopsis flexilis) showed very high but constant levels of organic acidity. This is frequently observed in C3/CAM intermediates when operating in C3 mode. The rates of net CO2 uptake during the day ranged from 1.4-24 μmol m2 s-1, thus covering the same range as found in tropical trees. The correlation of the maximum rates of net CO2 uptake and diel carbon balances was the same as previously found in other tropical species providing further evidence for the generality of this relationship.
Article
Gas exchange in Clusia rosea has been measured under various conditions of water status, light and leaf-air vapour pressure deficit (Δw, mbar bar−1) which produce daytime (C3), night-time (CAM) or 24 h uptake of CO2. At high light levels, at a Δw of 6.6, well-watered plants utilized C3 photosynthesis while CAM and 24 h uptake occurred under lower light levels and with low to normal water availability and differing Δw (13.5 and 3.4, respectively). CO2 uptake was highest, stomatal conductance to water vapour (gH2o) lowest, and water use efficiency (WUE) highest in plants using C3 photosynthesis. This latter fact is contrary to the accepted view that CAM is most water use efficient, i.e. it optimizes CO2 uptake with minimal water loss. It is suggested that the low CO2 uptake in CAM photosynthesis may be related not only to the higher Δw but also to the fact that Clusia species accumulate citrate which may originate from β-carboxylation of fatty acids (i.e. an internal source of CO2) and does not contribute to night-time external CO2 assimilation. Curves of assimilation (A) versus internal partial pressure of CO2 (A/c1) for the three photosynthetic types, under atmospheric conditions, did not produce a single trend. The trends which were produced represent the supply function for the interaction, under differing modes of photosynthesis, of the two major enzyme systems involved in CAM.
Article
Two case studies are presented illustrating how the behaviour of plants using crassulacean acid metabolism (CAM) provides adaptation to salinity. Perennial cacti having constitutive CAM show adaptation at the whole-plant level, engaging regulation of stomata, internal CO2-recycling and root physiology with salt exclusion. They are stress avoiders. Annual plants such as Mesembryanthemum crystallinum, with inducible CAM, are salt includers. They are stress-tolerant and show reactions at an array of levels: (i) regulation of turgor and gas exchange at the whole-plant level; (ii) metabolic adjustments at the cellular level; (iii) adapptive transport proteins at the membrane level and also (iv) at the macromolecular level; and (v) inductive changes at the gene expression level of the enzyme complement for metabolism (in particular involving glycolysis and malic-acid synthesis with phosphoenolpyruvate carboxylase (PEPC) as the key enzyme, and gluconeogenesis (with pyruvate–phosphate dikinase (PPDK) as a key enzyme) and membrane transport (in particular involving the tonoplast ATPase).
Article
Gas exchange and organic acid accumulation of the C3-CAM intermediate Clusia minor L. were investigated in response to various day/night temperatures and two light regimes (low and high PAR). For both light levels equal day/night temperatures between 20°C and 30°C caused a typical C3 gas exchange pattern with all CO2 uptake occurring during daylight hours. A day/ night temperature of 15°C caused a negative CO2 balance over a 24 h period for low-PAR-grown plants while high-PAR-grown plants showed a CAM gas exchange pattern with most CO2 uptake taking place during the dark period. However, there was always a considerable night-time accumulation of malic acid which increased when the night-time temperature was lowered and had its maximum (54 mmol m−2) at day/night temperature of 30/15°C. A significant amount of malic acid accumulation (23 mmol m−2) in low-PAR-grown plants was observed only at 30/15°C. Recycling of respiratory CO2 in terms of malic acid accumulation reached between 2·0 and 21·5 mmol m−2 for high-PAR-grown plants while there was no significant recycling for low-PAR-grown plants. Both low and high-PAR-grown plants showed considerable night-time accumulation of citric acid. Indeed under several temperature regimes low-PAR-grown plants showed day/night changes in citric acid levels whereas malic acid levels remained approximately constant or slightly decreased. It is hypothesized that low and high-PAR-grown plants have different requirements for citrate. In high-PAR-grown plants, the breakdown of citrate prevents photoinhibition by increasing internal CO2 levels, whereas in low-PAR-grown plants the night-time accumulation of citric acid may function as an energy and carbon saving mechanism.
Article
Full-text available
This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. Carbon isotope fractionation and nocturnal acid accumulation in Clusia osaensis Hammel-ined., C. peninsulae Hammel-ined. and C. valerii Standl. were investigated during the seedling, epiphytic and hemiepiphytic phases in a lowland tropical forest in Costa Ricato study photosynthetic adaptations of different plant growth stages to their habitat. Foliar δ 13C values around -24 to -32‰ indicate predominant C3 fixation of CO2 and low crassulacean acid metabolism (CAM) activity in all three Clusia species. Only terrestrially rooted plants of C. osaensis showed increased CAM expression. However, all developmental stages exhibited significant CAM cycling as shown by significant day-night fluctuations of titratable protons and of malic and citric acid. In C. valerii and C. peninsulae, an increase in CAM expression with plant development was not observed, and CAM cycling in hemiepiphytic-stage plants was completely repressed during the high rainfall season. The expression of CAM in the three Clusia species is therefore not developmentally controlled but triggered by environmental factors such as water availability and light intensity. These factors remain relatively stable in this ecosystem and CAM is therefore not fully expressed. However, CAM cycling may be of ecophysiological significance in all life stages as it serves as a mechanism to improve carbon economy by reducing respiratory CO2 losses.
Article
Wenn sich der Winter in die Hochlagen und den hohen Norden zurückgezogen hat, stellt manch einer seine Zimmerpflanzen ins Freie, um sie in den Genuß warmer Mairegen und des nun endlich eingetretenen „Wachswetters” zu bringen. Nur zu oft bewirkt diese gut gemeinte Behandlung aber den gegenteiligen Effekt. Die Blätter bekommen helle Flecken, vergilben, werden schließlich abgeworfen, und man darf froh sein, wenn die Pflanze noch Kraft genug hat, ein neues Blattkleid nachzutreiben. Was ist passiert?
Chapter
Since the discovery that Clusia lundellii is a CAM plant (Tinoco Ojanguren and Vásquez-Yánez 1983), species of Clusia have received considerable attention by plant ecophysiologists: first, because Clusia is one of the only genera amongst the Magnoliopsida (Dicotyledonae) that contain arborescent CAM species, and second, because some species of Clusia show substantial flexibility in the expression of CAM in response to the environment (Schmitt et al. 1988; Lee et al. 1989; Franco et al. 1990, 1991, 1992; Bail et al. 1991a, b; Borland et al. 1992; Haag- Kerwer et al. 1992; Winter et al. 1992) (see also Chaps. 15 and 19). In this chapter, we focus on Clusia uvitana Pitt., a hemiepiphytic species in the tropical moist forest of Barro Colorado Island (BCI), Panama (Croat 1978; Hammel 1986). Both epiphytic and hemiepiphytic plants, the latter possessing roots that reach the ground, can be found high up in the crowns of tall canopy trees, but also on rocks and tree trunks along the shoreline. C. uvitana is more abundant than C3 hemiepiphytes such as species of Ficus (Todzia 1986). This finding probably reflects advantages of CAM in a climate characterized by a pronounced dry season from mid-December to April. During this time, monthly rainfall is frequently less than 20 mm, while the average monthly rainfall during the wet season usually exceeds 150 mm (Windsor 1990).
Chapter
Full-text available
Climatic diversity between the Tropics of Cancer and Capricorn results from variation in the amount, seasonality, and distribution of rainfall, and from changes in evapotranspiration determined by altitudinal location in tropical mountains. This paper encompasses plant communities in the tropics growing in areas where rainfall is much higher than potential evapotranspiration during most of the year. A convenient separation of the wet and dry realms of tropical environments is provided by Bailey’s index, calculated from rainfall and average temperature data (Bailey, 1979). According to Bailey’s model, the lowland humid tropics are characterized by average annual temperatures around 26°C and average annual rainfall above 1500 mm. As the temperature decreases with increasing elevation in tropical mountains, the amount of rainfall required for humid climatic conditions also decreases. The sequence of lowland tropical forests that occurs along rainfall gradients, including dry woodlands at the lower end and rainforests at the higher end of rainfall, can also be observed along altitudinal gradients (Beard, 1944).
Article
Plectranthus marrubioides, a leaf succulent native to the Higher Escarpment of Yemen, shows obligate CAM. Even in the youngest leaves nocturnal accumulation of malic and, to a lower extent, of citric acid (≈ 10% that of malic acid) was measurable. Patterns of gas exchange were typically that of CAM plants in mature leaves while expanding leaves exhibited CAM-cycling. Gas exchange patterns were very flexible. In response to changes in the environmental conditions they could reversibly be switched between all variations of CAM. Decreasing daytime temperature from 35 to 20°C or varying light intensities from 150 to 600 μmol m⁻² S⁻¹ did not influence nocturnal CO2 uptake or malic acid accumulation but enhanced daytime carbon gain. Eliminating day/night temperature difference induced CAM-cycling, while changes in nighttime air humidity had no consequences for CAM. Withholding watering suppressed daytime carbon gain within 2 days but neither enhanced nor restricted CAM at moderate environmental conditions. Even at high temperature and low humidity it was reduced only partially with decreasing leaf water content; long-term drought led to CAM-idling. Leaf water content was highly correlated with malic acid accumulation under drought and over the age gradient. The only pronounced effect on nocturnal CO2 gain and malic acid accumulation was exhibited by nighttime temperature. Temperature response of CAM was influenced by the combination of environmental factors during both night and day. Thus, temperature optima ranged from 15 to 25°C in many experiments, resulting in a mean optimum of 20°C. The data show that it is mainly C3 photosynthesis and leaf conductance that flexibly responded to ecophysiological relevant changes in environmental conditions while CAM is much less affected.
Chapter
In the 57 years of research reviewed in this essay, transport functions were studied in a variety of plant systems. Processes of membrane transport are essential in the operation of various glands, such as nectary glands, the glands of carnivorous plants, and the salt glands of halophytes. In the photosynthetic mode of crassulacean acid metabolism (CAM), a central feature is nocturnal accumulation of organic acids in the vacuoles. Thus, CAM poses a transport problem, which was resolved by the identification of the complement of an H+-transporting ATPase, a malate channel, and a passive diffusion of non-dissociated malic acid at the tonoplast. The free running endogenous rhythm of CAM is operated by a biochemical-biophysical oscillator where the tonoplast acts as a master switch. The paths of transport with apoplastic and symplastic transport and diffusion in the gas phase of aerenchymas couple and integrate cells within tissues. The energization of membrane transport is linked to the multicomponent network of energy metabolism. Transport in roots and leaves was investigated to show this. All these features of plant biology indirectly or directly bear relations to physiological ecology of field performance. CAM is an ecophysiological adaptation to limited water supply which was studied intensively in the field in various tropical environments with respect to physiological autecology and ecosystem-relevant synecology. Whole-plant physiology shows that transport is the basis of the functioning of entire plants. Transport is the pathway for interaction and integration creating plant’s individuality as unitary organisms. The integration of modules via transport leads to the emergence of holistic systems across a large range of scalar levels from compartments within cells to cells and eventually the whole biosphere. Comprehending emergence of holism leads to understanding life beyond mechanistic modularity.
Chapter
Approximately 2000 articles on plant water relations published between 1987 and 1989 came to the notice of the author, the essential contents of 440 of them are mentioned in the following pages.
Chapter
One of the great fascinations of the genus Clusia is that its single leaf morphotype (Sect. 2.1) expresses different photosynthetic physiotypes. Often different photosynthetic types are even expressed by the same species and even in clones of vegetatively propagated plants or in different leaves of single individual plants depending on environmental conditions. The photosynthetic types observed among Clusias are based on the modes of C3-photosynthesis and of crassulacean acid metabolism (CAM) and its variants. Figure 8.1 presents a schematic overview of the basic features of the three to four different photosynthetic physiotypes found among Clusias. Figures 8.2 and 8.3 show typical patterns of photosynthetic CO2-gas exchange for different modes of photosynthesis expressed among four different species under identical conditions in a phytotron (Fig. 8.2) and for different modes of photosynthesis expressed in one species, Clusia minor L., under different conditions (Fig. 8.3), respectively.
Article
The large majority of the ca. 150 species of the neotropical shrub and tree genus Clusia have the potential to perform Crassulacean acid metabolism (CAM). They are either obligate CAM plants or C3/CAM intermediate plants. Only a very small percentage of the plants studied so far are apparently obligate C3 species. Among these was C. criuva, until recent laboratory studies showed that it may also have a certain CAM capacity under artificial stress conditions. Measurements of stomatal conductance (porometry) and chlorophyll fluorescence variables of C. criuva occurring along a transect from deep shade inside a gallery forest across the semi-shaded ecotone towards a cerrado and into the exposed cerrado itself in central Brazil now show that it can adapt its photosynthetic apparatus to effective performance of C3 photosynthesis under highly different photosynthetic photon flux densities. In addition, however, it does have a certain potential for CAM and cannot be considered as a strictly obligate C3 plant. Should a basic capacity for performing CAM be a general property of the genus, the quest for CAM traits in other remaining putatively obligate C3 species of the genus ought to be pursued.
Article
Plectranthus marrubioides, a leaf succulent native to the Higher Escarpment of Yemen, shows obligate CAM. Even in the youngest leaves nocturnal accumulation of malic and, to a lower extent, of citric acid (≃ 10% that of malic acid) was measurable. Patterns of gas exchange were typically that of CAM plants in mature leaves while expanding leaves exhibited CAM-cycling. Gas exchange patterns were very flexible. In response to changes in the environmental conditions they could reversibly be switched between all variations of CAM. Decreasing daytime temperature from 35 to 20°C or varying light intensities from 150 to 600 μmol m-2 s-1 did not influence nocturnal CO2 uptake or malic acid accumulation but enhanced daytime carbon gain. Eliminating day/night temperature difference induced CAM-cycling, while changes in nighttime air humidity had no consequences for CAM. Withholding watering suppressed daytime carbon gain within 2 days but neither enhanced nor restricted CAM at moderate environmental conditions. Even at high temperature and low humidity it was reduced only partially with decreasing leaf water content; long-term drought led to CAM-idling. Leaf water content was highly correlated with malic acid accumulation under drought and over the age gradient. The only pronounced effect on nocturnal CO2 gain and malic acid accumulation was exhibited by nighttime temperature. Temperature response of CAM was influenced by the combination of environmental factors during both night and day. Thus, temperature optima ranged from 15 to 25°C in many experiments, resulting in a mean optimum of 20°C. The data show that it is mainly C3 photosynthesis and leaf conductance that flexibly responded to ecophysiological relevant changes in environmental conditions while CAM is much less affected.
Chapter
IntroductionClimatePollutionWater DeficitSoil Conditions, Nutrient Deficiency/Enrichment and Soil DegradationConclusions AcknowledgementsReferences
Chapter
Diversity is probably best considered as a genetic criterion. It refers to the question: which genes are there?
Article
This study was carried out to investigate growth characteristics of woody plants that are widely used indoors in accordance with irrigation frequency and to find the optimum irrigation conditions for plants that help to improve the indoor environment. Four woody plants used in this study included Ardisia pusilla, Clusia rosea, Fatsia japonica, and Ficus elastica. They were planted in pots with a diameter of 10cm and cultivated in three different irrigation frequencies: two times per week, one time per week, and one time per two weeks. After 120 days, they were measured by plant height, fresh weight, dry weight, SPAD value, leaf color, leaf water potential, chlorophyll fluorescence (Fv/Fm), and photosynthetic rate. The average soil moisture content was 48.8±2.1% in two times per week, 25.2±4.4% in one time per week, and 10.3±2.4% in one time per two weeks. For A. pusilla, leaf water potential was higher, and Fv/Fm value was 0.731 in two times per week irrigation, showing more wetness. For A. pusilla, F. japonica and F. elastica photosynthetic rate was significantly lower in one time per two weeks irrigation, appearing to be more sensitive to drying than C. rosea. When irrigated one time per week, with the soil`s volume average moisture content of 25%, all four woody plants used in this experiment proved to grow smooth. Thus, it was determined to be good for use in indoor landscaping.
Chapter
The four phases of gas exchange, defined for CAM plants by Osmond in 1978, have provided the framework for the interpretation of physiological and biochemical studies on the regulation of this pathway in both constitutive and facultative CAM plants. Whilst the main CAM processes of dark uptake of CO2 and organic-acid decarboxylation occur during Phases I and III, respectively, the daytime Phases II and IV are often considered merely as transitions between C3 and C4 carboxylation. However, uptake of external CO2 during the day, particularly during Phase IV, contributes a substantial proportion of the assimilates used for the growth of consitutive CAM plants. In addition, daytime photosynthesis is essential for maintaining a positive carbon balance during the C3-CAM transition in facultative plants.
Article
The effects of water deficits on the growth and physiology of potted pitaya plants were examined in this study. Soil water decreased from 80% to 15% (severe deficit) over 16 weeks in non-irrigated pots, while stem water decreased from 90% to 80% (small deficit). Drought decreased final stem growth, chlorophylls, and Fv/Fm by 18% to 30% compared to the control. The stomata were mainly open from 1600 to 2400 h, with drought decreasing the percentage of stomata that were open and their aperture size. Starch grains accumulated in the chloroplasts during the day, with fewer starch grains under drought. Sugars and starch accumulated in the stem throughout the day and peaked at 2000 or 2400 h, while acids were lowest at 1600 h in the control. They were all significantly lower and relatively stable under drought. RUBPC activity peaked at 1200 h and PEPC activity at 2000 to 2400 h in the controls. Both were relatively stable with PEPC activity always lower under drought. Pitaya is a non-facultative CAM plant with strong ability to hold water under severe drought. Drought reduces short-term carbon production but does not appear to have a large effect on stem growth which possibly uses stored reserves.
Article
Clusia is a remarkable genus of Neotropical woody plants as its members engage in either C3 photosynthesis or employ, to varying degrees, crassulacean acid metabolism (CAM) photosynthesis. Information about the evolutionary history of CAM in Clusia is scarce. Restriction site-associated sequencing of 64 species (20% of the genus) provided strong support for most of the previously recognized nine lineages. Ancestral reconstruction using maximum parsimony or maximum likelihood under a one-rate model suggested that CAM evolved at least four times independently from a most recent common ancestor (MRCA) with C3, whereas a maximum likelihood two-rate model suggested that CAM was already present in the MRCA followed by reversions to C3 in several lineages. Phylogenetic generalized least square analysis assessed variation in seven leaf anatomical traits and CAM activity measured as δ 13C. Results indicate that CAM is highly correlated with palisade mesophyll layer thickness and cell size. In addition, correlation between 19 bioclimatic variables and δ 13C was evaluated. It was found that CAM is positively correlated with habitats with a more severe dry season and greater precipitation seasonality. Since CAM is weakly and/or only periodically expressed in many Clusia spp., and thus not readily reflected in δ 13C, future analysis of phylogenetically-informed CAM expression in Clusia must include physiological measurements such as CO2 exchange and/or diel changes in leaf acidity for each species under investigation.
Chapter
Full-text available
Crassulacean acid metabolism (CAM) is one of three metabolic pathways found in the photosynthetic tissues of vascular plants for assimilation of atmospheric CO2. In contrast to C3 and C4 plants, CAM plants take up CO2 from the atmosphere predominantly at night, subsequently assimilating this CO2 to the level of carbohydrate during the following light period. Elucidation of the complete pathway of carbon assimilation in CAM plants took nearly 150 years and encompassed many fundamental discoveries in plant biochemistry.
Chapter
Vines climb up. From a starting point in the forest understory, vines use the mechanical competence of neighboring plants in their ascent towards the bright sun of the forest canopy. Hemiepiphytes climb down. They begin life in the treetops and extend earthward to form permanent and often substantial connection with the soil (Figure 13.1). Vines and hemiepiphytes hold in common a period of mechanical dependence, yet the physiological consequences and constraints associated with this reliance upon external support differs substantially between the two groups. In vines, adaptations essential for effective climbing constrain their outward form and thus influence the uptake, transport, and storage of energy and materials. For hemiepiphytes, in contrast, the major constraints may not be the particular rigors associated with life as either an epiphyte or a tree, but rather in the plasticity required to succeed as both. Our discussion of tropical vine physiology is morphologically organized, considering in turn the function of stems, leaves, and roots. With hemiepiphytes, we focus primarily on the nature of the transition between the epiphytic and tree growth forms. We draw upon the roles of vines and hemiepiphytes in tropical forest communities only as such discussion provides insights into their physiology.
Chapter
Perhaps epiphytism could be thought to be primarily the utilization of any possible surface for holdfast and establishment, i.e. a conquest of space with epiphytes found in aquatic and terrestrial habitats made up of various combinations of lower and higher plants. In aquatic habitats, i.e. lakes, rivers and the sea, there are always algae growing on each other. This not only applies to unicellular and filamentous forms and their colonies, but also to macroalgae like kelp and red algae. In the mesic terrestrial climate many lower plants are epiphytic, like mosses and lichens and also some forms of small pleurococcoid aerial green algae as well as cyanobacteria (blue green algae). In the tropics lower plants may constitute massive formations of epiphytic biomass, e.g. the mosses in upper montane cloud forests (“moss-forests”, Fig. 4.1.).
Article
summaryClusia rosea Jacq. is abundant in the moist parts of the Caribbean island of St John (US Virgin Islands, Lesser Antilles) but relatively rare along the dry south coast. Three types of seedlings were encountered, terrestrial seedlings, seedlings growing as humus-epiphytes on other trees, and seedlings growing inside the tanks of the bromeliad Aechmea lingulata (L.) Baker. Free-living trees grow from terrestrial seedlings or from epiphytic seedlings strangling and shading their host trees. Leaf-Na+ levels were always low (1–4 mequiv I−1 tissue water); trees close to the shore were not affected by salinity. In leaves of mature C. rosea trees, levels of Ca2+, Mg2+ and K+ were about 60–90, 40–50, 45–55 mequiv I−1 tissue water, respectively. Epiphytic seedlings tended to contain lower levels of these inorganic cations than seedlings growing terrestrially or in the tanks of Ae. lingulata. Epiphytic seedlings contained significantly less nitrogen than terrestrial seedlings. In the leaves of mature trees N-levels were independent of altitude and location on the island, but shaded leaves had significantly higher N-levels than exposed leaves. Light compensation point of photosynthesis in epiphytic seedlings performing C3-photosynthesis was 17–5 (μmol photons m−2 s−1), photosynthesis was saturated at about 300μmol photons m−2 s−1 showing a maximum rate of CO2-uptake of 2–3 μmol m−2 s−1.
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Since the publication of the first edition of this book ten years ago, international research into the physiological ecology of plants in the tropics has increased enormously in quantity and quality. This brand new edition brings the story right up to date. New approaches have been developed in remote sensing. At the other end of the scale, molecular biology has come on in leaps and bounds, particularly regarding ecological performance of tropical plants, e.g. in understanding the adaptation of resurrection plants to the extreme habitat of inselbergs. In this fully revised and updated second edition the wealth of new information has made it necessary to break large chapters down into smaller ones. Tropical forests which occupy about half of the entire volume of the book are now arranged in five chapters covering structure and function under the influence of environmental cues and including epiphytes and mangroves as part of the tropical forest complex. Savannas are now treated in two chapters. Meanwhile, coastal salinas have been combined with a new section on the Brazilian restingas in a chapter on coastal sand plains.
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Hemiepiphytic species in the genera Clusia and Ficus were investigated to study their mode of photosynthetic metabolism when growing under natural conditions. Despite growing sympatrically in many areas and having the same growth habit, some Clusia species show Crassulacean acid metabolism (CAM) whereas all species of Ficus investigated are C3. This conclusion is based on diurnal CO2 fixation patterns, diurnal stomatal conductances, diurnal titratable acidity fluctuations, and 13C isotope ratios. Clusia minor, growing in the savannas adjacent to Barinas, Venezuela, shows all aspects of Crassulacean acid metabolism (CAM) on the basis of nocturnal gas exchange, stomatal conductance, total titratable acidity, and carbon isotope composition when measured during the dry season (February 1986). During the wet season (June 1986), the plants shifted to C3-type gas exchange with all CO2 uptake occurring during the daylight hours. The carbon isotope composition of new growth was-28 to-29 typical of C3 plants.
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Conductance for water vapor, assimilation of CO(2), and intercellular CO(2) concentration of leaves of five species were determined at various irradiances and ambient CO(2) concentrations. Conductance and assimilation were then plotted as functions of irradiance and intercellular CO(2) concentration. The slopes of these curves allowed us to estimate infinitesimal changes in conductance (and assimilation) that occurred when irradiance changed and intercellular CO(2) concentration was constant, and when CO(2) concentration changed and irradiance was constant. On leaves of Xanthium strumarium L., Gossypium hirsutum L., Phaseolus vulgaris L., and Perilla frutescens (L.), Britt., the stomatal response to light was determined to be mainly a direct response to light and to a small extent only a response to changes in intercellular CO(2) concentration. This was also true for stomata of Zea mays L., except at irradiances < 150 watts per square meter, when stomata responded primarily to the depletion of the intercellular spaces of CO(2) which in turn was caused by changes in the assimilation of CO(2).Stomata responded to light even in leaves whose net exchange of CO(2) was reduced to zero through application of the inhibitor of photosynthetic electron transport, cyanazine (2-chloro-4[1-cyano-1-methylethylamino]-6-ethylamino-S-triazine). When leaves were inverted and irradiated on the abaxial surface, conductance decreased in the shaded and increased in the illuminated epidermis, indicating that the photoreceptor pigment(s) involved are located in the epidermis (presumably in the guard cells). In leaves of X. strumarium, the direct effect of light on conductance is primarily a response to blue light.Stomatal responses to CO(2) and to light opposed each other. In X. strumarium, stomatal opening in response to light was strongest in CO(2) free air and saturated at lower irradiances than in CO(2) containing air. Conversely, stomatal closure in response to CO(2) was strongest in darkness and it decreased as irradiance increased. In X. strumarium, P. vulgaris, and P. frutescens, an irradiance of 300 watts per square meter was sufficient to eliminate the stomatal response to CO(2) altogether. Application of abscisic acid, or an increase in vapor pressure deficit, or a decrease in leaf temperature reduced the stomatal conductance at light saturation, but when the data were normalized with respect to the conductance at the highest irradiance, the various curves were congruent.
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Plants having crassulacean acid metabolism (CAM) tend to occupy habitats where the prevailing environmental stress is scarcity of water. These are semi-arid or arid regions, salinas or epiphytic sites. CAM plants manage the dilemma of desiccation or starvation by nocturnal malic acid accumulation in the vacuoles. Malic acid serves as a form of CO2 storage and as an osmoticum. In this way malic acid accumulation allows, firstly, separation of uptake and assimilation of atmospheric CO2 with water-saving daytime stomatal closure and, secondly, osmotic acquisition of water. There is no very special trait which is specific for CAM. An array of biophysical and biochemical functional elements, which are also found in other plants, is integrated in CAM performance. This leads to a large diversity of behaviour which makes CAM plants highly versatile in their response to environmental variables. Besides CO2 dark fixation, transport of malic acid across the tonoplast is one of the key elements in CAM function. This is examined in detail at the level of membrane biophysics and biochemistry. The versatility of CAM is illustrated by examples from field work, with comparisons involving different species, seasons, modes of photosynthesis (CAM vs C3), kinds of stress and ways of stress imposition.
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When the shrub Nerium oleander L., growing under full natural daylight outdoors, was subjected to water stress, stomatal conductance declined, and so did non-stomatal components of photosynthesis, including the CO2-saturated rate of CO2 uptake by intact leaves and the activity of electron transport by chloroplasts isolated from stressed plants. This inactivation of photosynthetic activity was accompanied by changes in the fluorescence characteristics determined at 77 K (-196°C) for the upper leaf surface and from isolated chloroplasts. The maximum (F M) and the variable (F V) fluorescence yield at 692 nm were strongly quenched but there was little effect on the instantaneous (F O) fluorescence. There was a concomitant quenching of the maximum and variable fluorescence at 734 nm. These results indicate an inactivation of the primary photochemistry associated with photosystem II. The lower, naturally shaded surfaces of the same leaves were much less affected than the upper surfaces and water-stress treatment of plants kept in deep shade had little or no effect on the fluorescence characteristics of either surface, or of chloroplasts isolated from the water-stressed leaves. The effects of subjecting N. oleander plants, growing in full daylight, to water stress are indistinguishable from those resulting when plants, grown under a lower light regime, are exposed to full daylight (photoinhibition). Both kinds of stress evidently cause an inactivation of the primary photochemistry associated with photosystem II. The results indicate that water stress predisposes the leaves to photoinhibition. Recovery from this inhibition, following restoration of favorable water relations, is very slow, indicating that photoinhibition is an important component of the damage to the photosynthetic system that takes place when plants are exposed to water stress in the field. The underlying causes of this water-stress-induced susceptibility to photoinhibition are unknown; stomatal closure or elevated leaf temperature cannot explain the increased susceptibility.
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The limitations on carbon dioxide assimilation by plants caused by stomata, particularly when the plant is under stress, are discussed. Mechanisms by which stomatal movement is integrated with photosynthesic requirements are described.
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The results described represent the first detailed measurements of gas exchange of epiphytic plants with crassulacean acid metabolism (CAM) in the humid tropics. A portable steady-state CO2 and H2O porometer was used to measure net exchange rates of CO2 and H2O vapour (JCO2, JH2O), leaf temperature (T1), air temperature (TA), air relative humidity (RH) and photosynthetically active radiation (PAR) for bromeliads in the field during the dry season in February and March 1983 on the tropical island of Trinidad. Different lengths of tubing (up to 25 m) were used so that the gas exchange could be measured of bromeliads in situ in their epiphytic habitats. Derived parameters such as leaf-air water-vapour-concentration difference (Δw), water-vapour conductance of leaves (g) and internal CO2 partial pressure (pⁱCO2) could be calculated.
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Clusia rosea Jacq. is a hemiepiphyte having Crassulacean Acid Metabolism (CAM). In its natural habitat Clusia begins its life cycle as an epiphyte and eventually becomes a rooted tree. These two stages of the life cycle of Clusia represent markedly different water regimes. Our CO2 exchange, stomatal conductance, titratable acidity, and stable carbon isotope ratio measurements indicate that Clusia has a flexible photosynthetic mode, where CO2 is fixed mostly via CAM during its epiphytic stage, when water availability is low, and via both CAM and C3 during its rooted stage.
Article
Lee, H. S. J. and Griffiths, H. 1987. Induction and repression of CAM in Sedurn relephluni L. in response to photopcnod and water stress.—J. exp. Bot. 38: 834–841. The introduction and repression of CAM in Sedurn telephiunm L, a temperate succulent, was investigated in watered, progressively drouglited and rewatered plants in growth chambers. Measurements were made of water vapour and CO2 exchange, titratable acidity (TA) and xylem sap tension. Effects of photoperiod were also studied. CAM was induced by drought under long or short days, although when watered no CAM activity was expressed. C3-CAM intermediate plants were used for the investigation of water supply. Those which had received water and those drought-stressed both displayed a similar nocturnal increase in TA, with a day-night maximum (δH+) of 69 μmol g−1 fr. wt. The watered plants took up CO2 at a maximum rate of 2·2 μmol m−2 s−1 only in the light period, while the droughted plants showed a maximum nocturnal CO2 uptake rate of 0·69 μmol m−2 s−1. Subsequently, as CAM was repressed, the watered S. telephiwn displayed little variation in TA, with constant levels at 42 μmol g−1 fr. wt. (day 10). After 10 d of drought stress, the CAM characteristics of S. telephiurn were aLso affected, with reduced net CO2 uptake and δH+. The transition between C3 and CAM in S. telephium can be described as a progression in terms of the proportion of respiratory CO2 which is recycled and refixed at night as malic acid, in comparison with net CO2 uptake. Recycling increased from 20% (day 1) to 44% (day 10) as a result of the drought stress and was high in both the CAM-C3 stage (no net CO2 uptake at night) and also in the drought-stressed CAM stage (reduced net CO2 uptake at night). The complete C3-CAM transition occurred in less than 8 d, and the stages could be characterized by xylem sap tension measurements: CAM = 0·50 MPa C3-CAM = 0·36 MPa C3 = 0·29 MPa.
Article
Observations of malic acid fluctuation, leaf anatomy, and stable carbon isotopic composition showed that the epiphytic strangler Clusia rosea, growing on Saint John, U.S. Virgin Islands, has crassulacean acid metabolism. This hemiepiphyte may be the only woody dicotyledonous tree species among the many thousands of flowering species in the 30 or more plant families that shows this type of metabolism. The finding has implications with respect to water balance during the process whereby Clusia rosea establishes itself as a tree, since crassulacean acid metabolism is a photosynthetic adaptation to water-stressed environments.