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VOCs – helping trees withstand global change?

2002; Wiley; Volume: 155; Issue: 2 Linguagem: Inglês

10.1046/j.1469-8137.2002.00461_1.x

1469-8137

Heinz Rennenberg, Jörg‐Peter Schnitzler,

Forest Insect Ecology and Management

The predicted increase in global temperature of c. 0.4°C per decade in the near future (Parry, 2001) will cause strong regional and temporal effects resulting in areas with more semiarid and/or more moderate climatic conditions. In Mediterranean regions especially, an increase in temperature accompanied by a reduction of precipitation is expected. This alteration in the physical environment will change the interspecific competition between plants with benefits for species better adapted to the predicted climatic conditions. Recently, strong evidence has emerged that the emission of volatile isoprenoids, such as the hemiterpene isoprene and monoterpenes can be an adaptive trait to increase the thermotolerance of several tree species (Sharkey & Yeh, 2001). The report by Peñuelas & Llusià (see pp. 227–237 in this issue) provides further support for this hypothesis and suggests, intriguingly, that the production of monoterpenes can replace photorespiration in the protection of leaves from photodamage at high temperatures. Monoterpenes constitute a major fraction of the biogenic volatile organic compounds (VOCs) emitted from vegetation (Guenther et al., 1995) and serve a wide range of functions in plants. In particular, the conifers, mint, citrus, and composite families accumulate these substances in ducts, glands and cavities. These isoprenoids are considered a means of defence against insects, fungi, herbivores and other plant species. When volatilised, monoterpenes can be signals for pollinators and conspecific herbivores, and can also mediate tritrophic interactions (Harborne, 1991). However, recent observations indicate that leaves of several tree species, such as the evergreen sclerophyllous holm oak (Quercus ilex), emit large amounts of monoterpenes despite the absence of storage pools (Loreto et al., 1998a). As demonstrated for isoprene (Sharkey & Yeh, 2001), this monoterpene emission is largely associated with photosynthesis. It is stimulated by light, declines in the dark, and is inhibited in the absence of atmospheric CO2 (Loreto et al., 1996a,b). The physiological function of the emission of nonstored monoterpenes from certain plant species is a matter of debate and an important topic of current research on biosphere–atmosphere exchange. In this respect, one of the most fascinating hypotheses is that monoterpenes may protect leaves against high-temperature damage (Sharkey & Singsaas, 1995; Loreto et al., 1998a). Even though this phenomenon has been demonstrated for several species, clear-cut evidence for the proposed mechanisms of this profound effect has not been achieved (Sharkey & Yeh, 2001). The emission of nonstored monoterpenes can be controlled by the rate of synthesis; hence, the balance of synthesis and evaporation determines the internal leaf concentration of isoprenoids (Fall, 1999). Because gaseous volatiles must pass through the stomata to exit the leaf, the tissue concentration can be strongly influenced by changes in stomatal opening. In the Mediterranean climate, where temperature extremes and aridity are more frequent, stomatal closure and strong, temperature-dependent increases in synthesis can build up high internal isoprenoid concentrations, as convincingly demonstrated in the work of Peñuelas & Llusià on holm oak. The observation that isoprenoid synthesis increases dramatically at high temperatures and results in high internal leaf concentrations led to the hypothesis that emitted isoprenoids may play a role in the thermal protection of plants. It was Sharkey and Singsaas (1995) who proposed for the first time that isoprene can protect photosynthesis from damage caused by high leaf temperatures. This hypothesis was further promoted by the observation that isoprenoid emission can increase the recovery of photosynthesis after short high-temperature episodes (Singsaas & Sharkey, 1998). This was concluded from experiments with isoprene-emitting plants by blocking isoprene biosynthesis with fosmidomycin, a specific inhibitor of the plastidal 2-C-methyl-D-erythritol 4-phosphate (MEP)-pathway, and by fumigation of leaves with exogenous isoprene while applying heat stress (Sharkey et al., 2001). Similar fumigation experiments have been performed with monoterpenes demonstrating that these isoprenoids also increase the thermotolerance of photosynthesis in the monoterpene-emitting evergreen oak (Quercus ilex) (Loreto et al., 1998b), as well as in the non-monoterpene-emitting cork oak (Q. suber) (Delfine et al., 2000; see also the accompanying commentary –Singsaas (2000)). The mechanism(s) by which this protection is achieved is still unclear. The currently favoured explanation is that volatile isoprenoids are embedded in membranes either serving as volatile mediators of biomembrane fluidity (Sharkey & Yeh, 2001) or preventing membrane lipid denaturation following oxidative stress (Loreto & Velikova, 2001; Loreto et al., 2001). Surprisingly little is known about the interrelationship between isoprenoid biosynthesis in plants and photorespiration. This is particularly true for the emission of monoterpenes. Early work of Jones & Rasmussen (1975) suggested that isoprene biosynthesis was linked to the photorespiratory cycle. This conclusion was supported by data showing an enhanced isoprene emission under low CO2 concentrations, conditions that are known to enhance photorespiration (Tingey et al., 1981). However, subsequent results with Populus tremuloides (Monson & Fall, 1989), Arundo donax (Hewitt et al., 1990) and Q. rubra (Delwiche & Sharkey, 1993) indicated that there was no close relationship between isoprene emission and photorespiration. The present report by Peñuelas & Llusià, (2002) opens a new view on the connection between photorespiration and monoterpene formation that is not focused only on photorespiration as an alternative source of carbon for isoprenoid biosynthesis when photosynthesis is limited. The importance of the work by Peñuelas and Llusià is its contribution to our understanding of the physiological mechanisms underlying monoterpene-related thermotolerance. It demonstrates that photorespiration seems to be necessary to avoid photochemical damage most notably under high temperature conditions. Moreover, it shows that leaf internal monoterpene accumulation and hence the formation of monoterpenes depends on the photorespiratory activity of the leaves. This gives strong evidence for the assumption that the leaf-internal carbon turnover in the photorespiratory cycle, even under high temperatures when stomata are closed, provides enough CO2 to keep the Calvin cycle and plastidic monoterpene biosynthesis via the (MEP)-pathway running. When fumigated with monoterpenes under nonphotorespiratory conditions, monoterpenes seem to replace photorespiration in the protection against high temperatures. This last observation of Peñuelas and Llusià, in particular, is of tremendous importance for future studies aimed at elucidating the role of monoterpenes as scavengers of reactive oxygen species and/or stabilisers of photosynthetic membrane–protein complexes, as well as the analysis of the competition for redox and energy equivalents between photorespiration and monoterpene biosynthesis.