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Leaf Anatomy and C02 Recycling During Crassulacean Acid Metabolism in Twelve Epiphytic Species of Tillandsia (Bromeliaceae)

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Leaf Anatomy and C02 Recycling During Crassulacean Acid Metabolism in Twelve Epiphytic Species of Tillandsia (Bromeliaceae) Int. J. Plant Sci. 154(1): 100-106. 1993. © 1993 by The University of Chicago. All rights reserved. 1058-5893/93/5401 -0010502.00 LEAF ANATOMY AND C02 RECYCLING DURING CRASSULACEAN ACID METABOLISM IN TWELVE EPIPHYTIC SPECIES OF TILLANDSIA (BROMELIACEAE) VALERIE S. LOESCHEN,* CRAIG E. MARTIN,' * MARIAN SMITH,t AND SUZANNE L. EDERf •Department of Botany, University of Kansas, Lawrence, Kansas 66045-2106; and t Department of Biological Sciences, Southern Illinois University, Edwardsville, Illinois 62026-1651 The relationship between leaf anatomy, specifically the percent of leaf volume occupied by water- storage parenchyma (hydrenchyma), and the contribution of respiratory C02 during Crassulacean acid metabolism (CAM) was investigated in 12 epiphytic species of Tillandsia. It has been postulated that the hydrenchyma, which contributes to C02 exchange through respiration only, may be causally related to the recently observed phenomenon of C02 recycling during CAM. Among the 12 species of Tillandsia, leaves of T. usneoides and T. bergeri exhibited 0% hydrenchyma, while the hydrenchyma in the other species ranged from 2.9% to 53% of leaf cross-sectional area. Diurnal malate fluctuation and nighttime atmospheric C02 uptake were measured in at least four individuals of each species. A significant excess of diurnal malate fluctuation as compared with atmospheric C02 absorbed overnight was observed only in T. schiedeana. This species had an intermediate proportion (30%) of hydrenchyma in its leaves. Results of this study do not support the hypothesis that C02 recycling during CAM may reflect respiratory contributions of C02 from the tissue hydrenchyma. Introduction tions continue through fixation of internally re• leased, respired C02 (Szarek et al. 1973; Ting Crassulacean acid metabolism (CAM) consti• 1985; Winter et al. 1986; Lee et al. 1989). This tutes a complex metabolic adaptation which re• process, termed "CAM-idling" (Ting 1985), may duces the possibility of drought stress in plants benefit a plant by preventing photoinhibition living in arid environments such as deserts, as (Osmond et al. 1980) or by maintaining meta• well as in the potentially stressful microenviron- bolic readiness during stress, enabling rapid re• ment of tropical epiphytes (Kluge and Ting 1978; covery once the stress is removed (Szarek et al. Osmond 1978; Winter 1985). Crassulacean acid 1973). metabolism plants reduce water loss by closing their stomata during the day when the temper• In other species, uptake of atmospheric C02 ature and vapor pressure deficit are high, and occurs throughout the day as in C3 plants, while opening their stomata during the night when the respiratory C02 is captured throughout the night evaporative demand of the atmosphere is lower. and, as in CAM plants, stored in the form of malate. Thus, malate accumulates at night while At night, atmospheric C02 is absorbed, resulting in the formation of malic acid, which is stored stomata are closed, and, hence, no atmospheric overnight in large vacuoles. During the day, mal• C02 is absorbed. The ecophysiological signifi• ate is released from the vacuoles and decarbox- cance of this form of intermediate metabolism, termed "CAM-cycling" (Ting and Rayder 1982; ylated; this C02 enters the photosynthetic carbon reduction cycle (Kluge and Ting 1978; Osmond Ting 1985), is poorly understood, although recent 1978; Winter 1985). work by Martin and co-workers suggests that this process may conserve water by reducing daytime In CAM, the stoichiometric ratio between moles transpiration (Martin et al. 1988; Harris and of malate formed and moles of C02 absorbed is Martin 1991). one (Kluge and Ting 1978). Therefore, integra• Most recently, another deviation from the 1:1 tion of C02 uptake rates throughout the night relationship between nocturnal malate formation should match the total amount of malate accu• and C02 uptake has been described for several mulated. In general, under nonstressful condi• species of epiphytic CAM plants (Griffiths et al. tions, this expected relationship has been ob• 1986; Smith et al. 1986; Griffiths 1988^) and a served in many CAM species (Medina and few terrestrial species (Sale and Neales 1980; Grif• Delgado 1976; Nobel and Hartsock 1978, 1983; fiths et al. 1986; Borland and Griffiths 1990). For Eickmeier 1979; Nobel et al. 1984; Winter et al. example, in the genus Tillandsia, 50%-90% of 1986; Virzo De Santo et al. 1987). Several vari• the nocturnally accumulated malate could not be ations have been observed, however, resulting in accounted for by the amount of atmospheric C02 divergence from the expected 1:1 stoichiometry. absorbed (Griffiths et al. 1986). These plants as• In terrestrial CAM plants under stress, stomata similate atmospheric C02 at night, while simul• remain closed day and night while acid fluctua- taneously fixing respiratory C02. In the current study, this phenomenon is referred to as "C02 1 Author for correspondence and reprints. recycling during CAM." It is actually surprising that all CAM plants do not exhibit C02 recycling Manuscript received September 1992; revised manuscript re• ceived November 1992. during CAM; apparently, rates of dark respiration 100 LOESCHEN ET AL.-C02 RECYCLING DURING CAM IN TILLANDSIA 101 are too slow to contribute measurable quantities enzuelana A. Richard, T utriculata L., and T of C02 to the buildup of malic acid in most CAM setacea Swartz were collected in the Everglades plants studied. There are at least two hypotheses region near the Big Cypress National Preserve why some CAM plants refix such high levels of east of Naples, Collier County, Florida. Most of respired C02 (Benzing 1990). Nighttime respi• these species were also collected from Taxodium ration rates may be higher in these species be• distichum, except T usneoides and T recurvata, cause of the warm tropical environment char• which were collected from Quercus virginiana acteristic of epiphytic CAM plants as compared Mill, and Quercus geminata Small, respectively. with terrestrial CAM plants in arid, temperate Tillandsia paleacea Presl and T bergeri Mez were regions (Winter et al. 1986; Luttge and Ball 1987; obtained from the collection at the Marie Selby Benzing 1990; Fetene and Luttge 1991). Many Botanical Gardens in Sarasota, Florida. Most terrestrial CAM plants, however, also grow in plants were collected in July and November 1988, tropical regions and do not exhibit C02 recycling although some were collected earlier. Nomencla• during CAM (Medina and Osmond 1981; Me• ture and authorities of the epiphytes are accord• dina 1982). Conversely, some CAM plants that ing to Smith and Downs (1977). reportedly recycle C02 through CAM grow in Plants were maintained in a greenhouse at the temperate regions (Borland and Griffiths 1990). University of Kansas under natural photoperiods Griffiths et al. (1986) have suggested that vari• with photosynthetic photon flux density (PPFD) 2 1 ations in leaf anatomy may explain this C02 re• between 500 and 1,000 ^mol m~ s" , depend• cycling phenomenon. Leaves of many of the epi• ing on time of day, location in greenhouse, and phytic CAM bromeliads that exhibit C02 recycling seasonal variability; day/night average air tem• during CAM have two distinct tissue types, wa• peratures of ca. 27/20 C (rarely maximum and ter-storage parenchyma ("hydrenchyma") and minimum temperatures of 38 and 10 C were re• chlorenchyma. The leaf volumetric ratio of hy• corded); and day/night relative humidities of ca. drenchyma : chlorenchyma varies widely among 50%/80%. Plants were watered three to five times epiphytic bromeliads, particularly among species per week, and a dilute solution of nutrients (18% of Tillandsia (Tomlinson 1969; Benzing and of each of total N, P2Os, K20; including trace Renfrow 1971). Hydrenchyma, lacking chloro• elements) was applied once per week. All plants phyll, should contribute C02 through respiration used in measurements appeared to be healthy, and might, in species with high hydrenchyma: growing, and some species occasionally flowered. chlorenchyma ratios, constitute a substantial LEAF TISSUE ANATOMY source of C02 for fixation by the adjacent chlo• renchyma tissue. Thus, an increase in the 1:1 Nine samples of midleaf sections of each spe• malate: C02 stoichiometry would be expected. cies were fixed in formalin-acetic acid-50% eth- The latter possibility has been investigated in anol (5:5:90, v/v/v), hand-sectioned, stained with two studies. Luttge and Ball (1987) reported rel• toluidine blue and mounted in water, and their atively minor contributions of C02 from the tis• images were projected with a Ken-A-Vision (Tech sue hydrenchyma to the total leaf dark respiration A II) microprojector onto white construction pa• in four terrestrial CAM plants. Griffiths (1988a), per using a 10 mm NA.25 lens. Leaf images were however, found greater amounts of C02 recycled traced and cut out, and the tissue ratios calculated during CAM in one epiphytic species of Aechmea by weighing the paper cut-outs of chlorenchyma that had a large amount of hydrenchyma tissue, and hydrenchyma. relative to another species in this genus with less hydrenchyma in its leaves. The possible effects GAS EXCHANGE of anatomy on C02 recycling during CAM in oth• Gas exchange of all species, with simultaneous er epiphytes remains unaddressed. We hypothe• sampling for malate, was measured from Decem• size that species with more hydrenchyma, rel• ber 1987 to December 1988 and additionally in ative to chlorenchyma, exhibit high levels of C02 November 1989 and December 1990 for T pa• recycling during CAM. leacea (Harris and Martin 1991). Nonliving ma• terial was removed; plants were wetted, allowed Material and methods to surface-dry (ca. 1 h), and weighed (species- average FW ranged from 2.5 to 14 g). Individuals STUDY SPECIES AND GROWTH CONDITIONS were sealed into temperature-controlled polycar• Individuals of Tillandsia schiedeana Steudel bonate chambers and allowed to acclimatize 1 d and T ionantha Planchon were collected from at 30/20 C day/night, 1,000-1,500 ^mol m~2 s"1 Taxodium distichum (L.) Rich, at El Salto Falls, PPFD inside the chambers (12-h photoperiod), San Luis Potosi, Mexico; T usneoides (L.) L., T and constant dew point of 15.5 C.
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