RESUMO
There is currently considerable interest in the prospects for bioengineering crassulacean acid metabolism (CAM) photosynthesis - or key elements associated with it, such as increased water-use efficiency - into C3 plants. Resolving how CAM photosynthesis evolved from the ancestral C3 pathway could provide valuable insights into the targets for such bioengineering efforts. It has been proposed that the ability to accumulate organic acids at night may be common among C3 plants, and that the transition to CAM might simply require enhancement of pre-existing fluxes, without the need for changes in circadian or diurnal regulation. We show, in a survey encompassing 40 families of vascular plants, that nocturnal acidification is a feature entirely restricted to CAM species. Although many C3 species can synthesize malate during the light period, we argue that the switch to night-time malic acid accumulation requires a fundamental metabolic reprogramming that couples glycolytic breakdown of storage carbohydrate to the process of net dark CO2 fixation. This central element of the CAM pathway, even when expressed at a low level, represents a biochemical capability not seen in C3 plants, and so is better regarded as a discrete evolutionary innovation than as part of a metabolic continuum between C3 and CAM.
Assuntos
Metabolismo Ácido das Crassuláceas , Fotossíntese , Dióxido de Carbono/metabolismo , Fotossíntese/fisiologia , Plantas/metabolismo , Água/metabolismoRESUMO
Guzmania monostachia (Bromeliaceae) is a tropical epiphyte capable of up-regulating crassulacean acid metabolism (CAM) in its photosynthetic tissues in response to changing nutrient and water availability. Previous studies have shown that under drought there is a gradient of increasing CAM expression from the basal (youngest) to the apical (oldest) portion of the leaves, and additionally that nitrogen deficiency can further increase CAM intensity in the leaf apex of this bromeliad. The present study investigated the inter-relationships between nitrogen source (nitrate and/or ammonium) and water deficit in regulating CAM expression in G. monostachia leaves. The highest CAM activity was observed under ammonium nutrition in combination with water deficit. This was associated with enhanced activity of the key enzyme phosphoenolpyruvate carboxylase, elevated rates of ATP- and PPi-dependent proton transport at the vacuolar membrane in the presence of malate, and increased transcript levels of the vacuolar malate channel-encoding gene, ALMT. Water deficit was consistently associated with higher levels of total soluble sugars, which were maximal under ammonium nutrition, as were the activities of several antioxidant enzymes (superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase). Thus, ammonium nutrition, whilst associated with the highest degree of CAM induction in G. monostachia, also mitigates the effects of water deficit by osmotic adjustment and can limit oxidative damage in the leaves of this bromeliad under conditions that may be typical of its epiphytic habitat.
Assuntos
Compostos de Amônio/metabolismo , Antioxidantes/metabolismo , Bromeliaceae/metabolismo , Malatos/metabolismo , Fotossíntese , Ascorbato Peroxidases/genética , Ascorbato Peroxidases/metabolismo , Transporte Biológico , Bromeliaceae/genética , Catalase/genética , Catalase/metabolismo , Secas , Regulação da Expressão Gênica de Plantas , Glutationa Redutase/genética , Glutationa Redutase/metabolismo , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Superóxido Dismutase/genética , Superóxido Dismutase/metabolismo , Água/metabolismoRESUMO
The key components of crassulacean acid metabolism (CAM) - nocturnal fixation of atmospheric CO2 and its processing via Rubisco in the subsequent light period - are now reasonably well understood in terms of the biochemical reactions defining this water-saving mode of carbon assimilation. Phenotypically, however, the degree to which plants engage in the CAM cycle relative to regular C3 photosynthesis is highly variable. Depending upon species, ontogeny and environment, the contribution of nocturnal CO2 fixation to 24-h carbon gain can range continuously from close to 0% to 100%. Nevertheless, not all possible combinations of light and dark CO2 fixation appear equally common. Large-scale surveys of carbon-isotope ratios typically show a strongly bimodal frequency distribution, with relatively few intermediate values. Recent research has revealed that many species capable of low-level CAM activity are nested within the peak of C3 -type isotope signatures. While questions remain concerning the adaptive significance of dark CO2 fixation in such species, plants with low-level CAM should prove valuable models for investigating the discrete changes in genetic architecture and gene expression that have enabled the evolutionary transition from C3 to CAM.
Assuntos
Adaptação Fisiológica , Evolução Biológica , Carbono/metabolismo , Fenótipo , Fotossíntese , Plantas , Água/metabolismo , Dióxido de Carbono/metabolismo , Isótopos de Carbono/metabolismo , Ecossistema , Genoma de Planta , Luz , Transpiração Vegetal , Plantas/genética , Plantas/metabolismoRESUMO
PREMISE OF THE STUDY: The fossil leaf Karatophyllum bromelioides L. D. Gómez found in Costa Rica was proposed by Gómez (1972) to belong to the Bromeliaceae and to date from the middle Tertiary. If the age and affinity of this specimen were proven to be correct, it would constitute the oldest record of this large and ecologically diverse monocotyledonous family. KEY RESULTS: Morphological features of the fossil (leaf dimensions, marginal spines, cuticular traces) indicate a close affinity with the extant bromeliad Aechmea magdalenae (André) André ex Baker. Leaf thickness (1.6 mm at maximum) suggests that K. bromelioides L. D. Gómez performed CAM photosynthesis. The geological information does not corroborate the estimated age and location of the specimen; the fossil is suggested to be of more recent origin. CONCLUSIONS: The affinity of this fossil to Bromeliaceae was confirmed, but the uncertainties surrounding its age and collection locality mitigate against its use in inferences concerning the evolutionary history of the family.
Assuntos
Bromeliaceae/classificação , Fósseis , Folhas de Planta/anatomia & histologia , Costa Rica , FotossínteseAssuntos
Evolução Molecular , Fotossíntese , Plantas/metabolismo , Dióxido de Carbono/metabolismo , Cloroplastos/metabolismo , Descarboxilação , Regulação da Expressão Gênica de Plantas , Genes de Plantas , Malatos/metabolismo , Mutação , Fenótipo , Fosfoenolpiruvato Carboxilase/metabolismo , Fotossíntese/genética , Folhas de Planta/metabolismo , Estômatos de Plantas/fisiologia , Plantas/genética , Elementos Reguladores de Transcrição , Ribulose-Bifosfato Carboxilase/metabolismo , Estresse FisiológicoRESUMO
The large Neotropical family Bromeliaceae presents an outstanding example of adaptive radiation in plants, containing a wide range of terrestrial and epiphytic life-forms occupying many distinct habitats. Diversification in bromeliads has been linked to several key innovations, including water- and nutrient-impounding phytotelmata, absorptive epidermal trichomes, and the water-conserving mode of photosynthesis known as crassulacean acid metabolism (CAM). To clarify the origins of CAM and the epiphytic habit, we conducted a phylogenetic analysis of nucleotide sequences for 51 bromeliad taxa by using the plastid loci matK and the rps16 intron, combined with a survey of photosynthetic pathway determined by carbon-isotope ratios for 1,873 species representing 65% of the family. Optimization of character-states onto the strict consensus tree indicated that the last common ancestor of Bromeliaceae was a terrestrial C(3) mesophyte, probably adapted to moist, exposed, nutrient-poor habitats. Both CAM photosynthesis and the epiphytic habit evolved a minimum of three times in the family, most likely in response to geological and climatic changes in the late Tertiary. The great majority of epiphytic forms are now found in two lineages: in subfamily Tillandsioideae, in which C(3) photosynthesis was the ancestral state and CAM developed later in the most extreme epiphytes, and in subfamily Bromelioideae, in which CAM photosynthesis predated the appearance of epiphytism. Subsequent radiation of the bromelioid line into less xeric habitats has led to reversion to C(3) photosynthesis in some taxa, showing that both gain and loss of CAM have occurred in the complex evolutionary history of this family.