Cladode development, environmental responses of CO2 uptake, and productivity for Opuntia ficus-indica under elevated CO2

Opuntia ficus-indica, an extremely productive CAM plant cultivatedin many countries, was exposed to 36, 52, and 72–73 PaCO₂ in field plots and open-top chambers. Initiation of newcladodes (stem segments) was monitored until the canopy closed,after which bimonthly harvests maintained the plants for oneyear at a cladode area per unit ground area that is optimalfor biomass production. Doubling the CO₂ partial pressure slightlyincreased the number of first-order daughter cladodes growingon the basal (planted) cladodes after 3 months and nearly doubledthe number and area of second-order cladodes. When the C02 levelwas doubled, cladodes were 5% thicker after a few months and11 to 16% thicker after one year. Although the productivityenhancement by elevated C02 tended to decrease during the year,the annual above-ground dry-mass gain was 37 to 40% higher whenthe C02 level was doubled, reaching 65 tons hectare^–1year^–1 in a field plot. Well-watered cladodes at day/nightair temperatures of 25°C/15°C and a total daily photosyntheticphoton flux (PPF) of 15 mol m^–2 d^–1 in controlledenvironment chambers had 74% more net CO₂ uptake over 24 h at73 Pa than at 37 Pa CO₂. With doubled CO₂, the percentage enhancementof net CO₂ uptake increased as the PPF was lowered, as the temperaturewas raised, and during drought. Using an environmental productivityindex based on such factors, net CO₂ uptake and hence productivityof O. ficus-indica can be predicted for elevated CO₂ levelsand other variations accompanying global climate change. Key words: Crassulacean acid metabolism, environmental productivity index, gas exchange, global climate change, plant growth     

Activities of carboxylating enzymes in the CAM species Opuntia ficus-indica grown under current and elevated CO2 concentrations

Responses of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPCase) to an elevated atmospheric CO₂ concentration were determined along with net CO₂ uptake rates for the Crassulacean acid metabolism species Opuntia ficus-indica growing in open-top chambers. During the spring 13 months after planting, total daily net CO₂ uptake of basal and first-order daughter cladodes was 28% higher at 720 than at 360 l CO₂ l^-1. The enhancement, caused mainly by higher CO₂ assimilation during the early part of the night, was also observed during late summer (5 months after planting) and the following winter. The activities of Rubisco and PEPCase measured in vitro were both lower at the elevated CO₂ concentration, particularly under the more favorable growth conditions in the spring and late summer. Enzyme activity in second-order daughter cladodes increased with cladode age, becoming maximal at 6 to 10 days. The effect ofelevated CO₂ on Rubisco and PEPCase activity declined with decreasing irradiance, especially for Rubisco. Throughout the 13-month observation period, O. ficus-indica thus showed increased CO₂ uptake when the atmospheric CO₂ concentration was doubled despite lower activities of both carboxylating enzymes.     

Environmental productivity indices and productivity for Opuntia ficus-indica under current and elevated atmospheric CO2 levels*

Abstract. The productivity of the prickly-pear cactus Opuntia ficus-indica, which is cultivated worldwide for its fruits and stem segments, was predicted based on the responses of its net CO₂ uptake to soil water status, air temperature and photosynthetic photon flux density (PPFD). Each of these environmental factors was represented by an index with a maximum value of unity when that factor was not limiting net CO₂ uptake over a 24-h period. The water index, the temperature index, and the PPFD index were determined for 87 sites in the contiguous United States using data from 189 weather stations and for 148 sites worldwide using data from 1464 weather stations. The product of these three indices, the environmental productivity index (EPI), was used to predict the productivity of O. ficus-indica under current climatic conditions and under those accompanying a possible increase in the atmospheric CO₂ level to 650μumol mol^?1. Sites with temperatures always above -10°C and hence suitable for prickly-pear cultivation numbered 37 in the United States and 110 worldwide; such sites increased by 43 and 5%, respectively, for the global warming accompanying the elevated CO₂. Productivity of O. ficus-indica was at least 15 tonnes dry weight hectare^?1 year^?1, comparable to that of many agronomic crops, for 20 sites with temperatures always above -10°C in the contiguous United States and for 12 such sites worldwide under current climatic conditions; such sites increased by 85 and 117%, respectively, under the elevated CO₂ condition, mainly because of direct effects of the atmospheric CO₂ level on net CO₂ uptake. In summary, simulations based on EPI indicate that O. ficus-indica may presently be advantageously cultivated over a substantial fraction of the earth's surface, such regions increasing markedly with a future doubling in atmospheric CO₂ levels.     

The origins of an important cactus crop, Opuntia ficus-indica (Cactaceae): new molecular evidence

Opuntia ficus-indica is a long-domesticated cactus crop that is important in agricultural economies throughout arid and semiarid parts of the world. The biogeographic and evolutionary origins of this species have been obscured through ancient and widespread cultivation and naturalization. The origin of O. ficus-indica is investigated through the use of Bayesian phylogenetic analyses of nrITS DNA sequences. These analyses support the following hypotheses: that O. ficus-indica is a close relative of a group of arborescent, fleshy-fruited prickly pears from central and southern Mexico; that the center of domestication for this species is in central Mexico; and that the taxonomic concept of O. ficus-indica may include clones derived from multiple lineages and therefore be polyphyletic.     

CO2 Exchange and Growth of the Crassulacean Acid Metabolism Plant Opuntia ficus-indica under Elevated CO2 in Open-Top Chambers

CO2 uptake, water vapor conductance, and biomass production of Opuntia ficus-indica, a Crassulacean acid metabolism species, were studied at CO2 concentrations of 370, 520, and 720 [mu]L L-1 in open-top chambers during a 23-week period. Nine weeks after planting, daily net CO2 uptake for basal cladodes at 520 and 720 [mu]L L-1 of CO2 was 76 and 98% higher, respectively, than at 370 [mu]L L-1. Eight weeks after daughter cladodes emerged, their daily net CO2 uptake was 35 and 49% higher at 520 and 720 [mu]L L-1 of C02, respectively, than at 370 [mu]L L-1. Daily water-use efficiency was 88% higher under elevated CO2 for basal cladodes and 57% higher for daughter cladodes. The daily net CO2 uptake capacity for basal cladodes increased for 4 weeks after planting and then remained fairly constant, whereas for daughter cladodes, it increased with cladode age, became maximal at 8 to 14 weeks, and then declined. The percentage enhancement in daily net CO2 uptake caused by elevated CO2 was greatest initially for basal cladodes and at 8 to 14 weeks for daughter cladodes. The chlorophyll content per unit fresh weight of chlorenchyma for daughter cladodes at 8 weeks was 19 and 62% lower in 520 and 720 [mu]L L-1 of CO2, respectively, compared with 370 [mu]L L-1. Despite the reduced chlorophyll content, plant biomass production during 23 weeks in 520 and 720 [mu]L L-1 of CO2 was 21 and 55% higher, respectively, than at 370 [mu]L L-1. The root dry weight nearly tripled as the C02 concentration was doubled, causing the root/shoot ratio to increase with CO2 concentration. During the 23-week period, elevated CO2 significantly increased CO2 uptake and biomass production of O. ficus-indica.     

Temperature influences on root growth for Encelia farinosa (Asteraceae), Pleuraphis rigida (Poaceae), and Agave deserti (Agavaceae) under current and doubled CO2 concentrations

To help evaluate root distribution patterns, elongation rates of individual roots were measured as a function of soil temperature for Encelia farinosa (a C₃ species), Pleuraphis rigida (C₄), and Agave deserti (CAM), sympatric codominants in the northwestern Sonoran Desert. Measurements were made at current and doubled CO₂ concentrations under winter and summer conditions of air temperature (day/night temperatures of 17 C/10 C and 33 C/22 C, respectively). The three species had different optimal temperatures for root elongation (T_opt) under winter conditions (25 C for E. farinosa, 35 C for P. rigida, and 30 C for A. deserti); T_opt increased by 2-3 C under summer conditions for all three species. The limiting temperatures for elongation also acclimated from winter to summer conditions. The rate of root elongation at T_opt was higher under summer than winter conditions for E. farinosa (9 vs. 6 mm d⁻¹) and P. rigida (20 vs. 14 mm d⁻¹), reflecting conditions for maximum photosynthesis; no difference occurred for A. deserti (9 vs. 10 mm d⁻¹). Decreased elongation rates at extreme temperatures were associated with less cell division and reduced cell extension. The doubled CO₂ concentration increased average daily root elongation rates for A. deserti under both winter (7%) and summer (12%) conditions, reflecting increased cell extension, but had no effect for the other two species. Simulations of root elongation as a function of soil temperatures showed that maximum elongation would occur at different depths (16-20 cm for E. farinosa, 4-8 cm for P. rigida, and 0-4 cm for A. deserti) and during different seasons (winter to spring for E. farinosa, spring to summer for P. rigida, and all year for A. deserti), contributing to their niche separation. Shading of the soil surface moderated daily variations in soil temperature, reducing seasonal root elongation for winter and spring and increasing elongation for summer. Shading also altered root distribution patterns, e.g., optimal rooting depth for A. deserti and especially P. rigida increased for a hot summer day.     

Phloem Exudate Collected via Scale Insect Stylets for the CAM Species Opuntia ficus-indica under Current and Doubled CO2 Concentrations

A method was devised for collecting phloem sap from the CAMspecies Opuntia ficus-indica using severed stylets of a scaleinsect (Dactylopius opuntiae), for which exudation could continuefor up to 5 d. For both basal (planted) cladodes and first-orderdaughter cladodes, the concentrations of sucrose and total aminoacids in the phloem exudate were virtually constant over 24-hperiods whereas the chlorenchyma osmolality had sizeable increasesduring the night under both current and doubled atmosphericCO₂ concentrations. Sucrose, total amino acids, and potassiumaccounted for 56, 21, and 9%, respectively, of the osmolalityof the phloem exudate, which was about 350 mOsm at the two CO₂concentrations; valine, isoleucine, leucine, tyrosine, glutamine,and lysine accounted for about 70% of the total amino acids.Doubling the CO₂ concentration led to approx. 5% more sucrose,560% more mannose and 17% less amino acids in the phloem exudateand also significantly increased mannose, starch and glucomannanin the chlorenchyma. Atmospheric CO₂ concentrations thus affectedvarious solute properties in the phloem and the chlorenchymaof O. ficus-indica.Copyright 1995, 1999 Academic Press Dactylopius opuntiae, Opuntia ficus-indica, cladode, CO₂ concentrations, Crassulacean acid metabolism, phloem exudate     

Irrigation magnifies CAM-photosynthesis in Opuntia basilaris (Cactaceae)

Summary Measurements of acid metabolism and gas exchange were carried out four times during a year to assess the relative importance of temperature and the accompanying seasonal change to the carbon metabolism of Opuntia basilaris Engelm. & Bigel. plants growing in situ under irrigated and natural (control) conditions. Our experiments showed that this cactus did not change its pattern of carbon assimilation when continuously irrigated under field conditions. Non-irrigated cacti had maximum acid accumulation after periods of precipitation. Maximum acid accumulation in irrigated cacti occurred when there was a large difference between day/night temperatures (i.e., 16°C), and when nighttime temperatures were moderate (14C). Irrigated cacti had greater duration of stomatal opening and lower resistance to ¹⁴CO₂ uptake. When temperatures were low, daytime stomatal resistance to ¹⁴CO₂ uptake decreased (to 20–40 s cm^-1), but never to the level of the nocturnal resistances (5–10 s cm^-1). During periods of drought, nonirrigated cycti changed to a pattern in which organic acids fluctuated. Irrigated cacti continued to have ¹⁴CO₂ uptake when nighttime temperatures were as high as 33°C. ¹³C/¹²C isotope composition ratios, determined after two years of irrigation, were near -12 in irrigated and non-irrigated plants. Therefore, under conditions of continual irrigation, seasonal and temperature changes affected the degree of dark CO₂ fixation and acid metabolism, but these cacti did not change from CAM to CO₂ fixation in the light.Abbreviations C₃ reductive pentose phosphate cycle - C₄ dicarboxylic acid cacle - CAE carbon assimilation efficiency - CAM Crassulacean acid metabolism - THO tritiated water - T/P transpiration ratio - vpd vapor pressure deficit - water potential This study was supported in part by National Science Foundation grant OIP 74-15673. Under the auspice of this grant a cooperative research project was carried out between the Australian National University, Canberra, and the Philip L. Boyd Deep Canyon Desert Research Center, University of California, Riverside. The studies involved a comparison of the photosynthetic pathways employed by succulents during growth in their native environment (the Sonoran Desert of southeastern California) and in a favorable introduced environment (Queensland and New South Wales, Australia). Studies carried out in Australia are under the direction of Dr. C.B. Osmond     

Opuntia fragilis (Cactaceae) verified in Illinois flora

Opuntia fragilis has been reported only once from Illinois. Recent workers have not been able to find a substantiating specimen and have excluded the species from the flora. The missing specimen has now been found and is referable to this species.     

Salt tolerance of prickly pear cactus (Opuntia ficus-indica)

In view of the need to exploit saline water resources in agriculture in arid zones, we investigated the salt tolerance of Opuntia ficus-indica in plants growing in solution culture. Salt (NaCl) was added in concentrations ranging from 5 (control) to 200 mol m^-3. Cladode growth was sensitive to salinity, being 60% of the control at 50 mol m^-3 NaCl. The root-to-stem ratio decreased significantly only at 200 mol m^-3. Various other parameters were studied, such as water content, Na, K and Cl content, osmotic pressure, and CO₂ uptake. Of these parameters the decreases in cladode water content and CO₂ uptake were related to the decrease in cladode growth. Raised salinity increased cladode osmotic pressure, which was associated with tissue dehydration. We concluded that osmotic adjustment does not occur in prickly pear under salt stress.     

Young daughter cladodes affect CO2 uptake by mother cladodes of Opuntia ficus-indica

BACKGROUND AND AIMS: Drought damages cultivated C3, C4 and CAM plants in the semi-arid lands of central Mexico. Drought damage to Opuntia is common when mother cladodes, planted during the dry spring season, develop young daughter cladodes that behave like C3 plants, with daytime stomatal opening and water loss. In contrast, wild Opuntia are less affected because daughter cladodes do not develop on them under extreme drought conditions. The main objective of this work is to evaluate the effects of the number of daughter cladodes on gas exchange parameters of mother cladodes of Opuntia ficus-indica exposed to varying soil water contents. METHODS: Rates of net CO2 uptake, stomatal conductance, intercellular CO2 concentration, chlorophyll content and relative water content were measured in mature mother cladodes with a variable number of daughter cladodes growing in spring under dry and wet conditions. KEY RESULTS: Daily carbon gain by mother cladodes was reduced as the number of daughter cladodes increased to eight, especially during drought. This was accompanied by decreased mother cladode relative water content, suggesting movement of water from mother to daughter cladodes. CO2 assimilation was most affected in phase IV of CAM (late afternoon net CO2 uptake) by the combined effects of daughter cladodes and drought. Rainfall raised the soil water content, decreasing the effects of daughter cladodes on net CO2 uptake by mother cladodes. CONCLUSIONS: Daughter cladodes significantly hasten the effects of drought on mother cladodes by competition for the water supply and thus decrease daily carbon gain by mother cladodes, mainly by inhibiting phase IV of CAM.     

Past and present role of the Indian-fig prickly-pear (Opuntia ficus-indica (L.) Miller,Cactaceae) in the agriculture of sicily

Of prickly-pear cacti occurring in Sicily, the most widespread and economically important isOpuntia ficus-indica (L.) Miller. In Sicily it has, since its introduction, played an important role in the exploitation of marginal areas. The Sicilian experience is described with reference to the historical outlines and the present intensive production of late fruit. Information on historical and actual uses of the plant and its products (flowers, cladodes, fruits) is given.     

CO(2) Fixation in Opuntia Roots

Nonautotrophic CO₂ metabolism in Opuntia echinocarpa roots was studied with techniques of manometry and radiometry. The roots were grown in a one-quarter strength nutrient solution for several days; the distal 2 cm was used for physiological studies. The roots assimilated significant quantities of ¹⁴CO₂ and appeared to show a crassulacean-type acid metabolism with respect to quality and quantity. Most of the ¹⁴C activity was associated with the distal portion of the elongating root indicating correlation with metabolic activity. The ¹⁴CO₂ assimilation was comparable to a crassulacean leaf succulent, but 3 times greater than that found for stem tissue of the same Opuntia species.

The rates of O₂ and CO₂ exchange and estimated CO₂ fixation were 180, 123, and 57 μl/g per hour. A respiratory quotient of 0.66 was found.

The products of ¹⁴CO₂ fixation were similar in most respects to reported experiments with leaf succulents. Equilibration of the predominant malic acid with isocitric, succinic, and fumaric acids was not evident. The latter observation was interpreted as metabolic isolation of the fixation products rather than poor citric acid cycle activity.

A rapid turnover of the fixed ¹⁴CO₂ was measured by following decarboxlyation kinetics and by product analysis after a postincubation period. The first order rate constant for the steady state release was 4.4 × 10⁻³ min⁻¹ with a half-time of 157.5 minutes. Amino acids decayed at a more rapid rate than organic acids.

     

Relationships between Photosynthetically Active Radiation, Nocturnal Acid Accumulation, and CO(2) Uptake for a Crassulacean Acid Metabolism Plant, Opuntia ficus-indica

The influences of photosynthetically active radiation (PAR) and water status on nocturnal Crassulacean acid metabolism (CAM) were quantitatively examined for a widely cultivated cactus, Opuntia ficus-indica (L.) Miller. When the total daily PAR was maintained at 10 moles photons per square meter per day but the instantaneous PAR level varied, the rate of nocturnal H⁺ accumulation (tissue acidification) became 90% saturated near 700 micromoles per square meter per second, a PAR level typical for similar light saturation of C₃ photosynthesis. The total nocturnal H⁺ accumulation and CO₂ uptake reached 90% of maximum for a total daily PAR of about 22 moles per square meter per day. Light compensation occurred near 0 moles per square meter per day for nocturnal H⁺ accumulation and 4 moles per square meter per day for CO₂ uptake. Above a total daily PAR of 36 moles per square meter per day or for an instantaneous PAR of 1150 micromoles per square meter per second for more than 6 hours, the nocturnal H⁺ accumulation actually decreased. This inhibition, which occurred at PAR levels just above those occurring in the field, was accompanied by a substantial decrease in chlorophyll content over a 1-week period.

A minimum ratio of H⁺ accumulated to CO₂ taken up of 2.5 averaged over the night occurred for a total daily PAR of 31 moles per square meter per day under wet conditions. About 2 to 6 hours into the night under such conditions, a minimum H⁺-to-CO₂ ratio of 2.0 was observed. Under progressively drier conditions, both nocturnal H⁺ accumulation and CO₂ uptake decreased, but the H⁺-to-CO₂ ratio increased. A ratio of two H⁺ per CO₂ is consistent with the H⁺ production accompanying the conversion of starch to malic acid, and it apparently occurs for O. ficus-indica when CAM CO₂ uptake is strongly favored over respiratory activity.

     

Genetic transformation of prickly-pear cactus (Opuntia ficus-indica) by Agrobacterium tumefaciens

A system for genetic transformation of an elite prickly pear cactus (Opuntia ficus-indica L., cultivar Villa Nueva) by Agrobacterium tumefaciens was developed. Beginning with direct bacterial infection by using a hypodermic syringe to the meristematic tissue termed areoles, transgenic plants were obtained by selection with 100 mg l⁻¹ kanamycin. Transient and stable GUS activities were monitored on kanamycin-resistant shoots and regenerated plants, respectively. Genetic transformation of regenerated plants growing under selection was demonstrated by PCR and Southern blot analysis; transgene copy number in the genome of transgenic plants ranged from two to six, while the transformation frequency obtained by the system reported here was of 3.2%. This method may be useful for routine transformation and introduction of several important genes in prickly pear cactus.     

Rapid propagation of tuna (Opuntia ficus-indica) and plant establishment in soil

Explants from young joints of mature plants of tuna (Opuntia ficus-indica Mill.) were cultured on Murashige and Skoog (MS) medium containing 8.8 M benzyladenine (BA) and 0.5 M naphthaleneacetic acid (NAA). Shoots produced were utilized as secondary explants. Each shoot was cut longitudinally from apex to base into two explants, and some of these explants were cut transversely into proximal and distal explants. The size and number of shoots produced was affected by size and position of the explant within its source. The shoots were rooted in vitro or ex vitro and plants were successfully established in soil from both rooting methods.Abbreviations AC activated charcoal - BA benzyladenine - IBA indolebutyric acid - MS Murashige & Skoog (1962) medium - NAA naphthaleneacetic acid     

Biomechanics and anatomy of cladode junctions for two Opuntia (Cactaceae) species and their hybrid

Hybridization between the introduced arborescent Opuntia ficus-indica and the native shrubby O. littoralis has led to populations, referred to as O. "occidentalis," which form thickets that can dominate hillsides of chaparral and that can survive fires. Because the thickets apparently develop via vegetative reproduction, O. "occidentalis" was hypothesized to have a greater ability than its parent species to reproduce vegetatively due to weaker cladode junctions. Of the three taxa, the junctions for O. "occidentalis" had the least amount of wood, despite having cladode masses and junction cross-sectional areas similar to those of O. littoralis. The cladodes of O. "occidentalis" resisted deflection about their junctions the least and their junctions required the least amount of applied mass and the smallest bending moment to fail mechanically. The junction wood for all three taxa consisted mostly of parenchyma, with lesser amounts of cells with thickened secondary cell walls, indicating that some junction strength depended on hydrostatic pressure, especially for terminal junctions. Libriform fibers, which contribute to support and resist bending moments, were about 80% less frequent in the sub-subterminal junctions of O. "occidentalis" than in O. ficus-indica and O. littoralis. Vascular tracheids, which probably reduced shear among cells in the wood, were 90% less frequent in the terminal and sub-subterminal junction wood of O. "occidentalis" compared to O. littoralis. Thus wood characteristics can account for the weaker junctions of O. "occidentalis" compared to those of O. ficus-indica and O. littoralis, which apparently increases the ability of the hybrid to reproduce vegetatively.     

Aborted fruits of Opuntia microdasys (Cactaceae): insurance against reproductive failure

New individuals in clonal populations arise through the recruitment of sexual or clonal offspring. The predominance of one type of regeneration over the other has been correlated with different selective environmental pressures. We compared the reproductive mode (sexual through seeds and vegetative through plantlets or detached cladodes) of Opuntia microdasys from three desert habitats of the Chihuahuan Desert: bajada (BH), hill-piedmont (HPH), and an interdune (IDH). Successful establishment and growth of plantlets were determined in two experiments: (1) the effect of light (three levels of photosynthetically active radiation [PAR]: full, low, and medium) and two levels of watering and (2) maternal effects and provenance of plantlets. Adult plant densities did not differ among habitats (639 individuals/ha), but the number of offspring and fruit production increased significantly at BH. Plantlets (94.3%) dominated the form of recruitment for all habitats, followed by cladodes (3.1%) and seedlings (2.6%). A higher proportion of plantlets established in the low and medium PAR treatments (76%) in comparison to full exposure (39%). Maternal factors affected survival and growth, but plantlet provenance did not. The high fruit abortion rate resulting from environmental and maternal effects provided suitable conditions for establishment of plantlets.