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Ecophysiology and Reproductive Biology of Cultivated Cacti

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Ecophysiology and Reproductive Biology of Cultivated Cacti 04 Ecophysiology and reproductive biology of cultivated cacti Paolo Inglesea,Giorgia Liguoria and Erick de la Barrerab a Department of Agricultural and Forestry Sciences, University of Palermo, Italy b Institute of Research in Ecosystems, National Autonomous University of Mexico, Mexico City, Mexico Ecophysiology and reproductive biology 04 of cultivated cacti INTRODUCTION Mojave Desert in California, or the Rajasthan Desert in India (Felker and Inglese, 2003). Le Houérou (2002) de- Cactus pear − Opuntia fcus-indica (L.) Mill. − is a CAM scribes plantations in Aziza (Lybia) where the maximum (crassulacean acid metabolism) plant cultivated in a wide temperature may exceed 50° C. O. fcus-indica cladode range of environments, resulting in major differences in cannot survive at 70° C (Nobel, 2002). plant survival and development, and in crop potential. The fruits of O. fcus-indica can be harvested from July The ecological success of opuntias, specifcally O. f- to November in the Northern Hemisphere − Mediterra- cus-indica, is due largely to their peculiar daily pattern nean Basin, California, and Mexico − and from January of carbon uptake and water loss, both of which occur to April in the Southern Hemisphere, depending on mostly at night. Like other CAM plants, cactus pear the genotype and genotype × environment interac- opens its stomata at night to fx CO2 and accumulate tion. Natural or induced refowering may extend the and store malate in the vacuoles of the chlorenchyma ripening period to January-February in the Northern cells. Since night-time temperatures are lower than di- Hemisphere and to September-October in the South- urnal ones, and relative humidity is generally higher, the ern Hemisphere. Almost continuous fowering has been transpiration of CAM plants is three to fve times lower reported in Salinas, California (Bunch, 1996), resulting than that of C3 and C4 plants (Nobel, 1988). The result in an extended fruit ripening period. is a tremendous increase in water-use effciency and in the plant’s ability to thrive in semi-arid environments characterized by a restricted water supply (200-300 mm CAM CYCLE of annual rainfall) or where long periods of drought and relatively high temperatures occur. The mechanisms of Originally attributed to the Crassulaceae family, CAM adaptation to aridity are not necessarily valid in relation represents a mechanism of concentration of CO which to high temperatures. Although they occur at night, CO 2 2 has evolved in response to dryness in terrestrial envi- uptake and acid accumulation are strongly infuenced by ronments and defciency of inorganic carbon in water environmental variables such as air temperature, light, environments (Keeley, 1998). plant water status, nutrients and soil salinity (Nobel, 1988). Indeed, in the native area of the Central Mexican CAM occurs in 16 000 species (6–7% of plant species), Plateau (1 800–2 200 m asl), rainfall is < 500 mm, the belonging to over 300 genera from around 40 families, mean annual temperatures range from 16 to 18° C, and ranging from the deciduous tropical forest to desert the daily maximum temperature for the hottest month platyopuntias and columnar cacti. The vast majority does not exceed 35° C (Pimienta Barrios, 1990). of plants using CAM are angiosperms. Most of them are either epiphytes (e.g. orchids, bromeliads) or suc- In the Mexican mesas (tablelands), the dry season coin- culent xerophytes (e.g. cacti, cactoid Euphorbias); but cides with a cold winter, while the hot season, during CAM is also found in lithophytes, terrestrial bromeliads, which fruit and vegetative growth take place, is very the halophyte Mesembryanthenum crystallynum, one humid and rainy; exactly the opposite occurs in the non-succulent terrestrial plant (Dodonaea viscosa) and Mediterranean Basin, where the dry season coincides one mangrove associate (Sesuvium portulacastrum). with the hottest days, when the fruit develops and veg- etative growth occurs (Inglese et al., 2002b). In Sicily, Characteristics of CAM and succulence where O. fcus-indica is grown for fruit production, annual rainfall is around 500 mm and the mean annual • Separation of CO uptake and decarboxylation − temperature ranges from 15 to 18° C, with peaks of 2 temporally or spatially. 37° C in August, during the fruit development period (Inglese, 1995). O. fcus-indica occurs extensively in • Reduction of transpiration due to night-time stomatal northern Africa (Monjauze and Le Houérou, 1965a), in opening − and water storage organs contain 90-95% the highlands (2 000-2 500 m asl) of Tigray, Ethiopia water compared with 40-70% of non-succulent wood. and in South Africa. In contrast, it is absent in regions • Reduced water loss − CAM plants lose 20-30% of with rainfall < 350 mm and daily summer maximum the water lost by C3 o C4 plants for the same degree temperatures > 42° C, such as the Sahelian belt, the of stomatal opening during daytime CO2 uptake. Ecophysiology and reproductive biology of cultivated cacti 31 • Low root: shoot ratios and fast root growth dur- • Phase 2. Early in the morning, the transition ing wet conditions. takes place from PEPc to Rubisco activity. • Suberization of cortical cells, with the formation • Phase 3. During the day, plants close their guard of root-soil gaps during soil drying. cells, stomata are tightly closed and the pH in- • Internal recycle of water from parenchyma vs creases. Malate diffuses out of the vacuole and is decarboxylated. CO is released (rising from 0.2 chlorenchyma − maintains turgor of the photosyn- 2 thetic tissue over a wide range of water content. to 2.5%) in the cytosol and fxed into the Calvin cycle in the chloroplasts by the ribulose-1,5-bis- • Supply of water and solutes to fruit through phosphate carboxylase/oxygenase (Rubisco) lead- phloem (phloem osmotic pressure is relatively ing to the synthesis of starch or other glucans. low: 0.94 MPa (2-3 times less than for most • Phase 4. In the late afternoon PEPc becomes other vascular plants). active. Under very dry environmental conditions, The CAM pathway can be summarized as follows this may be the only phase of the CAM cycle (Figure 1): that takes place. • Phase 1. At night, CO2 fxation occurs when sto- Measurements of gas exchange in O. fcus-in- mata open and CO2 diffuses into the mesophyll’s dica began in the early 1980s, when Nobel and intracellular spaces and then into the cytosol, Hartsock (1983) measured CO2 uptake on single where it is bound to phosphoenolpyruvate (PEP), cladodes. At optimal temperature and intercepted a 3-C compound, through PEP carboxylase. The radiation, instantaneous values of net CO2 uptake enzyme catalyzes the formation of oxaloacetate, of 1-year cladodes may reach 18 µmol m–2 s–1, with which can be transformed into malate by NAD+ –2 a total daily CO2 uptake of 680 mmol m (Nobel malate dehydrogenase. To avoid inhibition, and Bobich, 2002). However, although individu- malate is actively transported from the cytosol to al-cladode net photosynthesis (Pn) determinations the vacuole, where it is converted into malic acid, are useful for estimating gas exchange rate per unit leading to a noticeable increase in acidity. The area, they have limitations when used to scale up vacuoles of the cells of the chlorenchyma occupy to whole canopy gas exchange, because there may more than 90% of the cell volume because of be wide variability in carbon assimilation within the nocturnal accumulation of organic acids. canopy, due to differences in cladode age (Samish Figure 1 Light Dark Light Dark Light Dark Crassulacean acid metabolism (CAM) Carboydrate Triose phosphate Carboydrate breakdown Starch PCR cycle Phosphoglycerate Phosphoenolpyruvate pH Malate CO2 Pyruvate Total organic acids Oxaloacetate Malic Krebs cycle Malate Citric Stomata Stomata CO2 closed open 32 Crop ecology, cultivation and uses of cactus pear and Ellern, 1975), intercepted radiation (Nobel, 1988), • Root: shoot ratio ranges from 0.12 (Nobel, 1988) to crop load (Inglese et al., 1994b), source–sink relation- 0.09 (Inglese et al., 2012) and 0.20 (Inglese et al., ships (Pimienta Barrios et al., 2005) and response to 2012) on mature irrigated trees. abiotic stress (Nobel and Bobich, 2002). • Wax layer in the epidermis is 10-50 μm vs 0.2-2 μm in leaves of C3 or C4. Few data are available on cladode net CO2 uptake ac- cording to cladode age. Samish and Ellern (1975) noted • The chlorenchyma of O. fcus-indica can reversibly lose that titratable acidity decreases linearly with increasing 70% of its water content at full turgor and the parenchy- age, and 1-year cladodes have a level of acidity three ma can lose 82%, both still being able to fully recover. times higher than 2-year cladodes, located in a basipe- • After a 15-week drought period, the parenchyma tal position. Carbon translocation from 2-year cladodes loses 60% of its water content and the chlorenchyma to meet the photo-assimilate demand of 1-year fruiting 25% (Goldstein et al., 1991). cladodes has been hypothesized (Inglese et al., 1994b; De la Barrera and Nobel, 2004), and carbon partition- Sunny better than cloudy ing between mother and daughter cladodes changes depending on the cladode developmental stage and • Light and CO2 uptake are shifted in time and noctur- environmental conditions (shading, water availability) nal stomata opening depends on daily rather than (Luo and Nobel, 1993; Pimienta Barrios et al., 2005). instantaneous PPF values. CO2 uptake of 2-year cladodes throughout the season • Compensation point at PPF = 3 moles m−2 day−1. can be 40% lower than for 1-year cladodes (Liguori et • Saturation point at PPF = 30 moles m−2 day−1. al., 2013a). −2 −1 • At PPF = 22 moles m day , CO2 uptake is at 90% of its maximal. CAM-related statistics • O. fcus-indica may assimilate 344–680 mmol m−2 day−1 of CO (C = 35%).
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