Crassulacean acid metabolism under global climate change

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(Author for correspondence: tel +52 999 9428330; fax +52 999 9813900; email creyes@cicy.mx)

Crassulacean acid metabolism plant species as markers of global climatic change. A symposium within the Second National Ecology Meeting, Mexican Scientific Society of Ecology, Merida, Mexico, November 2008

The crassulacean acid metabolism (CAM) pathway evolved in response to stress, particularly to low-water supply or to low-CO2 supply. In nonaquatic plants the CAM pathway is usually accompanied by several mechanisms to cope with drought and high temperatures. Therefore, this curious metabolism could represent a competitive advantage under current climate change, where predictions in tropical areas are higher temperatures and longer droughts (IPCC, 2007). The symposium ‘Crassulacean Acid Metabolism Plant Species as Markers of Global Climatic Change’, recently took place within the Second National Ecology Meeting of the Mexican Scientific Society of Ecology (SCME), Merida, Mexico. In this symposium, the role of CAM plants under climatic change was discussed, from genetic, physiological and ecological perspectives.

‘If some orchid species have already walked part of the evolutionary path towards CAM, will current climate change drive their full conversion to the CAM pathway?’

Will CAM plants expand their range as a result of climate change?

Crassulacean acid metabolism is a carbon-concentrating mechanism where stomata open mainly at night, when driving forces for transpiration are low, thus minimizing water loss. The CO2 is initially fixed by the enzyme phosphoenolpyruvate carboxylase (PEPC) and stored in organic acids. During the day, the acids are broken down and the carbon available is used by the enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in the Calvin cycle. Early studies on the effect of climate change on vegetation focused on the response to increased CO2 concentrations. Surprisingly, long-term experiments showed a higher CO2 uptake in CAM plants that was not down-regulated with time, as occurred in most C3 species studied (Drennan & Nobel, 2000). Thus, in synergy with the carbon-concentrating mechanism, high CO2 concentrations stimulated higher afternoon carbon fixation by Rubisco. Nevertheless, it has become evident that other changing climatic factors, such as the rise in temperatures and longer droughts, are having strong effects on vegetation and are driving species out of their normal habitat range (Lenoir et al., 2008). At increased temperatures, photorespiration has been blamed for the reduced growth rates observed in tree species from tropical forests since the early 1970s (Clark et al., 2003; Feeley et al., 2007). J. Carlos Cervera and Louis S. Santiago (University of California Riverside, USA) described how CAM plants, with reduced photorespiration as a result of a high internal CO2 concentration, can have maximum photosynthetic rates at high temperatures (up to 54°C), and for cacti species of the Mojave desert in California, models of realized and predicted niches showed possible range expansion for some species. However, the expansion of cacti species (Opuntia basilaris and Mammillaria dioica) would be limited by other nonclimatic factors, such as low recruitment from sexual reproduction, dependence on specific birds as pollinators and the low mobility of the asexual offspring, which, along with habitat discontinuity and the velocity of climatic change, restricts the expected range expansion (Fig. 1). When all of these physiological and ecological aspects are considered, it seems that acclimation of these resistant species to their new conditions, rather than habitat mobility, is a more plausible scenario, assuming that other vital species, such as pollinators and nurse plants, also manage to acclimate. Nonetheless, some cacti, such as the prickly pear (Opuntia ficus-indica), with its high photosynthetic rate and high ability to colonize new environments (Osmond et al., 2008), could more easily show range expansion.

Figure 1.

Driving forces towards range expansion, local extinction or conserved population range for crassulacean acid metabolism (CAM) cacti. The direction of the arrows shows the tendency to move towards the three scenarios under climate change, indicated as higher temperatures and different rain patterns.

Some CAM plants show higher metabolic flexibility, failing to commit to a fully CAM or C3 status; they fluctuate from one metabolism to the other in response to environmental cues. The genus Clusia, which comprises arborescent species with reported CAM, has several species with a C3/CAM mode that can be found in a great variety of habitats and life forms (Lüttge, 2008). The flexible C3/CAM species can increase their total carbon gain by opening stomata during both day and night (Winter et al., 2008). José Luis Andrade (Centro de Investigación Científica de Yucatán, Mexico) explained how Clusia species showing CAM have more conservative water-use strategies than C3 species, and rapidly close stomata during drought, which can quickly limit water loss. Improved water use and flexibility to switch from the more productive C3 photosynthesis to the more conservative CAM, could determine survival and provide a higher competitive advantage over co-existing C3 tree species.

Can the natural variation in our CAM plant populations determine species survival under a rapidly changing climate?

In the family Orchidaceae, about 50% of the species have evolved varying degrees of CAM (strong or weak, depending on the proportion of total carbon fixed by CAM) from C3 ancestors (Silvera et al., 2005). Katia Silvera (University of Nevada-Reno, USA) described a genetic study on the evolution of Orchidaceae showing that a series of steps must occur from ancestral C3 photosynthesis to CAM, from anatomical changes (succulence allows accumulation of acids in vacuoles) to genetic duplication of relevant genes. Evolutionary steps towards CAM occurred independently, multiple times within the family. Moreover, genetic studies show that some currently weak CAM species already have the required genetic duplication, but have probably not completed all the anatomical steps towards CAM. Silvera and colleagues found a correlation between altitude and CAM occurrence, suggesting that a set of climatic drivers are determining CAM evolution. If some orchid species have already walked part of the evolutionary path towards CAM, will current climate change drive their full conversion to the CAM pathway?

The natural genetic variation found within populations can allow the survival of some individuals in the face of a devastating event such as disease or prolonged drought. Such is the case in a population of the CAM species Agave striata growing in Miquihuana, Mexico. Alfredo Huerta-de la Garza (University of Miami, USA) explained how half of this A. striata population presents red leaves covered with subepidermal anthocyanins and a thick cuticle; the other half of the population has green leaves that lack this photoprotective pigment. Work conducted in the Huerta-de la Garza laboratory showed that red leaves have higher light reflectance and higher quantum efficiency during the day, in comparison with green leaves. Under the predicted climatic scenario of longer droughts and higher ultraviolet radiation as a result of ozone depletion, it is plausible that the red phenotype will become more abundant because photoprotection is more valuable to a stressed plant than the extra light absorption the green phenotype achieves.

Can cacti spines and bromeliad leaves substitute tree rings in paleoclimate models of the tropics?

To understand future changes in climate and its effects on plant physiology, one approach is to study past climates in an attempt to establish differences in plant growth during hot and dry years. The proportion of the oxygen-stable isotopes (18O/17O, δ18O) in rainfall changes in response to temperature and humidity at the time of condensation, and this isotopic signal is recorded in plant cellulose. Models using the δ18O signal in tree rings have been created to reconstruct the rain signal at the time of cellulose synthesis, and with it climate. Examples of semifossilized cellulose used in these models are as old as 45 million years (Richter et al., 2008). As the different components that affect the cellulose δ18O are considered, a high uncertainty lies in the influence of the δ18O of atmospheric vapor. There is a general lack of field data on the effect of δ18O of atmospheric vapor because of the difficulty in trapping field samples. Helliker & Griffiths (2007) found that CAM epiphytic bromeliads, because they lack root contact with soil and perform gas exchange under conditions of high humidity, store the δ18O signal of atmospheric vapor in their cellulose. Casandra Reyes-García (Centro de Investigación Científica de Yucatán, Mérida, Yucatán, México) confirmed that CAM bromeliads from dry environments are good markers of atmospheric δ18O (Reyes-García et al., 2008) but did not observe the same relationship in CAM bromeliads from wet environments, showing water reservoirs in between their leaves, or in those bromeliads with C3 metabolism, where cellulose δ18O bore more resemblance to rain δ18O.

Tropical trees do not show annual growth rings, making it difficult to calculate their age and limiting their use to model paleoclimate. However, Nathan B. English (University of Arizona, USA) explained how spines of the cacti Carnegiae gigantea have transversal bands that correspond to days, and given the steady growth rate, it is possible to calculate age from these. The δ18O and 13C signatures of the spines revealed variation that coincides with diurnal or annual changes in rainfall and humidity over a 22-yr period, making cacti good models for reconstruction of climate in tropical areas (English et al., 2007).

Outlook

There have been enormous advances in ecophysiology since the early 1970s as a result of the significant increase in available technology. However, in tropical areas, where diversity is high, there are still significant gaps in knowledge. Given the complexity of tropical communities, there are few studies that encompass both the physiological changes caused by environmental factors and those caused by interaction with co-existing organisms, which would be needed to help predict community responses to climate change.

At this meeting, there was a special session conducted by Erick de la Barrera to introduce and comment on the new book ‘Perspectives in biophysical plant ecophysiology: a tribute to Park S. Nobel’ edited by E. De la Barrera and W. K. Smith (2009). The book includes works of 29 ecophysiologists that have been inspired by the very productive researcher Park S. Nobel. Nobel pioneered the use of physics to explain physiological processes and devoted most of his work to CAM species. The book represents a great example of the advances of ecophysiology in the last decade, and the future prospects section included in each chapter points the way towards the open questions in this expanding field.

Acknowledgements

We thank the SCME board for facilitating the organization of the CAM Symposium; the presenters for sharing their ongoing research; useful discussions with Drs Louis S. Santiago and Erick De la Barrera; and funding by CICY and CONABIO (GU002) and by a SEP-CONACYT grant (48344/24588) to JLA, for travel expenses of some of the presenters.

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