The diverse diaspora of CAM – a pole-to-pole sketch

Background: CAM photosynthesis is a successful adaptation that has evolved often in angiosperms, gymnosperms, ferns and lycophytes. Present in ca. 5 % of vascular plants, the CAM diaspora includes all continents barring Antarctica. Species with CAM inhabit most landscapes colonized by vascular plants, from the Arctic Circle to Tierra del Fuego, from below sea-level to 4,800 m, from rainforests to deserts. They have colonised terrestrial, epiphytic, lithophytic, palustrine and aquatic systems developing perennial, annual or geophyte strategies that may be structurally arborescent, shrub, forb, cladode, epiphyte, vine or leafless with photosynthetic roots. CAM may enhance survival by conserving water, trapping carbon, reducing carbon loss and/or via photoprotection. Scope: This review assesses the phylogenetic diversity and historical biogeography of selected lineages with CAM viz. ferns, gymnosperms and eumagnoliids, Orchidaceae, Bromeliaceae, Crassulaceae, Euphorbiaceae, Aizoaceae, Portulacineae (Montiaceae, Basellaceae, Halophytaceae, Didiereaceae, Talinaceae, Portulacaceae, Anacampserotaceae, Cactaceae) and aquatics. Conclusions: Most extant CAM lineages diversified since the Oligocene/Miocene as the planet dried and CO2 concentrations dropped. Radiations exploited changing ecological landscapes including Andean emergence, Panamanian Isthmus closure, Sundaland emergence and submergence, changing climates and desertification. Evidence remains sparse for or against theories that CAM-biochemistry tends to evolve prior to pronounced changes in anatomy, and that CAM tends to be a culminating xerophytic trait. In perennial taxa, any form of CAM may occur depending upon the lineage and the habitat, although facultative CAM appears uncommon in epiphytes. CAM annuals lack strong CAM. In CAM annuals, C3+CAM predominates and inducible- or facultative- CAM are common

Nocturnal versus diurnal CO2 uptake: how flexible is Agave angustifolia?

Agaves exhibit the water-conserving crassulacean acid metabolism (CAM) photosynthetic pathway. Some species are potential biofuel feedstocks because they are highly productive in seasonally dry landscapes. In plants with CAM, high growth rates are often believed to be associated with a significant contribution of C3 photosynthesis to total carbon gain when conditions are favourable. There has even been a report of a shift from CAM to C3 in response to overwatering a species of Agave. We investigated whether C3 photosynthesis can contribute substantially to carbon uptake and growth in young and mature Agave angustifolia collected from its natural habitat in Panama. In well-watered plants, CO2 uptake in the dark contributed about 75% of daily carbon gain. This day/night pattern of CO2 exchange was highly conserved under a range of environmental conditions and was insensitive to intensive watering. Elevated CO2 (800 ppm) stimulated CO2 fixation predominantly in the light. Exposure to CO2-free air at night markedly enhanced CO2 uptake during the following light period, but CO2 exchange rapidly reverted to its standard pattern when CO2 was supplied during the subsequent 24h. Although A. angustifolia consistently engages in CAM as its principal photosynthetic pathway, its relatively limited photosynthetic plasticity does not preclude it from occupying a range of habitats, from relatively mesic tropical environments in Panama to drier habitats in Mexico

Does the C4 plant Trianthema portulacastrum (Aizoaceae) exhibit weakly expressed crassulacean acid metabolism (CAM)?

We examined whether crassulacean acid metabolism (CAM) is present in Trianthema portulacastrum L. (Aizoaceae), a pantropical, salt-tolerant C 4 annual herb with atriplicoid-type Kranz anatomy in leaves but not in stems. The leaves of T. portulacastrum are slightly succulent and the stems are fleshy, similar to some species of Portulaca, the only genus known in which C 4 and CAM co-occur. Low- level nocturnal acidification typical of weakly expressed, predominantly constitutive CAM was measured in plants grown for their entire life-cycle in an outdoor raised garden box. Acidification was greater in stems than in leaves. Plants showed net CO 2 uptake only during the light irrespective of soil water availability. However, nocturnal traces of CO 2 exchange exhibited curved kinetics of reduced CO 2 loss during the middle of the night consistent with low-level CAM. Trianthema becomes the second genus of vascular land plants in which C 4 and features of CAM have been demonstrated to co-occur in the same plant and the first C 4 plant with CAM-type acidification described for the Aizoaceae. Traditionally the stems of herbs are not sampled in screening studies. Small herbs with mildly succulent leaves and fleshy stems might be a numerically significant component of CAM biodiversity

Operating at the very low end of the crassulacean acid metabolism spectrum: Sesuvium portulacastrum (Aizoaceae)

Demonstration of crassulacean acid metabolism (CAM) in species with low usage of this system relative to C₃-photosynthetic CO₂ assimilation can be challenging experimentally but provides crucial information on the early steps of CAM evolution. Here, weakly expressed CAM was detected in the well-known pantropical coastal, leaf-succulent herb Sesuvium portulacastrum, demonstrating that CAM is present in the Sesuvioideae, the only sub-family of the Aizoaceae in which it had not yet been shown conclusively. In outdoor plots in Panama, leaves and stems of S. portulacastrum consistently exhibited a small degree of nocturnal acidification which, in leaves, increased during the dry season. In potted plants, nocturnal acidification was mainly facultative, as levels of acidification increased in a reversible manner following the imposition of short-term water-stress. In drought-stressed plants, nocturnal net CO₂ exchange approached the CO₂-compensation point, consistent with low rates of CO₂ dark fixation sufficient to eliminate respiratory carbon loss. Detection of low-level CAM in S. portulacastrum adds to the growing number of species that cannot be considered C₃ plants sensu stricto, although they obtain CO₂ principally via the C₃ pathway. Knowledge about the presence/absence of low-level CAM is critical when assessing trajectories of CAM evolution in lineages. The genus Sesuvium is of particular interest because it also contains C₄ species

Intra‐cultivar potential of Desmanthus spp. as a greenhouse gas mitigation strategy for tropical livestock pastoral systems

Improved agricultural efficiency and reduction in the impacts of tropical livestock farming on habitat degradation require global approaches that enhance ruminant farming functionality in terms of feed use efficiency, emissions and food security. This study evaluated the in vitro mitigation potential of the prostrate to erect, herbaceous Desmanthus spp. pasture legume adapted to semiarid clay soil land types in northern Australia. D. bicornutus, D. leptophyllus and D.virgatus were seasonally harvested from commercial plots by Agrimix Pty. Ltd. Samples of the legumes and the control Rhodes grass (Chloris gayana) using ruminal fluid from grazing Brahman (Bos indicus) steers were incubated in vitro (Ankom RF1 Technology) for 24, 48 and 72 h. Overall, the in vitro organic matter degradability (OMD) and methane production between Desmanthus species differed (P < 0.001). Compared to the control (0.656 ± 0.027 proportion of total OM) at 48 h of incubation, D. leptophyllus showed lower OMD (0.479 ± 0.016), while D. bicornutus (0.688 ± 0.016) and D. virgatus (0.619 ± 0.015) were different from each other, but similar to the control. Methane production (ml/g OM) was 15.7 ± 1.54, 3.7 ± 0.89, 12.0 ± 0.95 and 11.7 ± 0.95, respectively. It is suggested that the impact of these attributes may benefit household farmers in developing economies to expand productivity, improve livelihoods and meet the growing food consumption. Further analyses of the intra‐cultivar characteristics of Desmanthus spp. will complement the design of sustainable and efficient interventions across tropical pastoral feeding systems, with a particular emphasis on large‐scale grazing operations

Environment or Development? Lifetime Net CO(2) Exchange and Control of the Expression of Crassulacean Acid Metabolism in Mesembryanthemum crystallinum

The relative influence of plant age and environmental stress signals in triggering a shift from C(3) photosynthesis to Crassulacean acid metabolism (CAM) in the annual halophytic C(3)-CAM species Mesembryanthemum crystallinum was explored by continuously monitoring net CO(2) exchange of whole shoots from the seedling stage until seed set. Plants exposed to high salinity (400 mm NaCl) in hydroponic culture solution or grown in saline-droughted soil acquired between 11% and 24% of their carbon via net dark CO(2) uptake involving CAM. In contrast, plants grown under nonsaline, well-watered conditions were capable of completing their life cycle by operating in the C(3) mode without ever exhibiting net CO(2) uptake at night. These observations are not consistent with the widely expressed view that the induction of CAM by high salinity in M. crystallinum represents an acceleration of preprogrammed developmental processes. Rather, our study demonstrates that the induction of the CAM pathway for carbon acquisition in M. crystallinum is under environmental control

How Closely Do the δ(13)C Values of Crassulacean Acid Metabolism Plants Reflect the Proportion of CO(2) Fixed during Day and Night?

The extent to which Crassulacean acid metabolism (CAM) plant δ(13)C values provide an index of the proportions of CO(2) fixed during daytime and nighttime was assessed. Shoots of seven CAM species (Aloe vera, Hylocereus monocanthus, Kalanchoe beharensis, Kalanchoe daigremontiana, Kalanchoe pinnata, Vanilla pauciflora, and Xerosicyos danguyi) and two C(3) species (teak [Tectona grandis] and Clusia sp.) were grown in a cuvette, and net CO(2) exchange was monitored for up to 51 d. In species exhibiting net dark CO(2) fixation, between 14% and 73.3% of the carbon gain occurred in the dark. δ(13)C values of tissues formed inside the cuvette ranged between −28.7‰ and −11.6‰, and correlated linearly with the percentages of carbon gained in the light and in the dark. The δ(13)C values for new biomass obtained solely during the dark and light were estimated as −8.7‰ and −26.9‰, respectively. For each 10% contribution of dark CO(2) fixation integrated over the entire experiment, the δ(13)C content of the tissue was, thus, approximately 1.8‰ less negative. Extrapolation of the observations to plants previously surveyed under natural conditions suggests that the most commonly expressed version of CAM in the field, “the typical CAM plant,” involves plants that gain about 71% to 77% of their carbon by dark fixation, and that the isotopic signals of plants that obtain one-third or less of their carbon in the dark may be confused with C(3) plants when identified on the basis of carbon isotope content alone

Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentrations of CO2

Do short-term fluctuations in CO2 concentrations at elevated CO2 levels affect net CO2 uptake rates of plants? When exposed to 600 µl CO2 l–1, net CO2 uptake rates in shoots or leaves of seedlings of two tropical C3 tree species, teak (Tectona grandis L. f.) and barrigon [Pseudobombax septenatum (Jacq.) Dug.], increased by 28 and 52% respectively. In the presence of oscillations with half-cycles of 20 s, amplitude of ca. 170 µl CO2 l–1 and mean of 600 µl CO2 l–1, the stimulation in net CO2 uptake by the two species was reduced to 19 and 36%, respectively, i.e. the CO2 stimulation in photosynthesis associated with a change in exposure from 370 to 600 µl CO2 l–1 was reduced by a third in both species. Similar reductions in CO2-stimulated net CO2 uptake were observed in T. grandis exposed to 40-s oscillations. Rates of CO2 efflux in the dark by whole shoots of T. grandis decreased by 4.8% upon exposure of plants grown at 370 µl CO2 l–1 to 600 µl CO2 l–1. The potential implications of the observations on CO2 oscillations and dark respiration are discussed in the context of free-air CO2 enrichment (FACE) systems in which short-term fluctuations of CO2 concentration are a common feature

Facultative crassulacean acid metabolism (CAM) in four small C-3 and C-4 leaf-succulents

Measurements of whole-plant gas exchange and titratable acidity demonstrate that the Australian native species Anacampseros australiana J.M.Black (Anacampserotaceae), Crassula sieberiana (Schult. & Schult.f.) Druce (Crassulaceae) and Portulaca australis Endl. (Portulacaceae) and the widespread naturalised tropical exotic, Portulaca pilosa L., exhibit facultative crassulacean acid metabolism (CAM). In well-watered plants, net CO2 uptake was restricted to the daylight hours and occurred via the C-3 pathway (A. australiana and C. sieberiana) or the C-4 pathway (P. australis and P. pilosa). Leaves of well-watered plants did not accumulate titratable acidity during the night. Following drought treatment, CO2 uptake in the light by shoots decreased markedly, nocturnal gas-exchange shifted from net CO2 loss to a CAM-type pattern that included net CO2 uptake, and leaves acidified at night. Nocturnal CO2 uptake by shoots and leaf acidification were most pronounced in A. australiana and least so in C. sieberiana. The induction of dark CO2 uptake and tissue acidification was fully reversible in all four species: upon rewatering, nocturnal CO2 uptake and acidification ceased and the rates of CO2 incorporation in the light were restored. Wesuggest that, hitherto considered relatively exceptional globally, facultative CAM may be more common than previously suspected, particularly among the generally small ephemeral leaf-succulents that characterise Australia's succulent flora

Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns

Crassulacean acid metabolism (CAM) was observed in three species of tropical ferns, the epiphytes Microsorium punctatum and Polypodium crassifolium and the lithophyte Platycerium veitchii. Polypodium crassifolium and P. veitchii exhibited characteristics of weak CAM. Although no net nocturnal CO2 uptake was observed, the presence of CAM was inferred from nocturnal increases in titratable acidity of 4.7 and 4.1 μequiv (g fr wt)–1 respectively, a reduction in the rates of net CO2 evolution during the first half of the dark period, and the presence of a CAM-like decrease in net CO2 uptake during the early light period. In M. punctatum net CO2 uptake during the first half of the dark period was accompanied by an increase in titratable acidity of 39.2 μequiv (g fr wt)–1 and a pronounced reduction in net CO2 uptake during the early light period. When water was withheld from P. crassifolium and M. punctatum, net CO2 uptake during the light was reduced markedly but there was no change in the extent or patterns of CO2 exhange in the dark. As a consequence, the proportion of carbon gained due to CO2 fixation in the dark increased from 2.8 and 10% to 63.5 and 49.3%, respectively (100% being net CO2 uptake during the light plus the estimated CO2 uptake during the dark). After 9 days without added water, dark CO2 uptake was responsible for the maintenance of a net 24 h carbon gain in P. crassifolium. Platycerium veitchii, P. crassifolium and M. punctatum exhibited carbon isotope ratios of between –25.9 and –22.6‰ indicating that carbon isotope ratios may not, by themselves, be sufficient for the identification of weak CAM. We suggest that CAM may be more prevalent in tropical epiphytic and lithophytic ferns than currently envisaged