論文の公開元へAre differences among forest tree populations in carbon isotope composition an indication of adaptation to drought?
概要
Plants have developed different strategies to cope with a reduced water availability in the soil (Levitt 1980). Drought resistance of forest trees is mainly a question of survival and competition within an ecosystem. However, in forestry, it is also a question of maintaining growth. Functional traits can be termed ‘adaptive’ to drought, providing that their genetic variation can be linked to an increased fitness under soil water deficit conditions. The observation of trees grown from seeds of different populations in one or several common environments (e.g., provenance trials or common garden experiments) is a means to control for environmental variation, and therefore to detect genetic differences among these different populations, and potentially genotype × environment interactions, if trials are replicated at different locations. Populations from different environments may differ in their mean values of any functional trait in the sense that these mean values relate to the environmental differences of the original population sites. This can be taken as a first indication that these traits are involved in the adaptation of populations to the local conditions. Studying population differences involves measuring the phenotypes of large numbers of individual plants. In this context, the carbon isotope composition (δ13C) of plant organic material has been widely used.
δ13C variations of plant organic matter reflect variations in intrinsic water-use efficiency (Wi, the ratio between A, the net CO2 assimilation rate and gs, the stomatal conductance to water vapor). This relationship has been explained by Farquhar et al. (1989) using a mechanistic model of CO2 fluxes in the leaf and isotopic fractionation factors. Some of the model parameters—listed in Figure 1—are likely to vary across genotypes or populations and could therefore weaken the relationship between δ13C and Wi. A number of publications on forest trees have nevertheless shown a strong relationship between these two traits, either when comparing provenances (Grossnickle et al. 2005, Ducrey et al. 2008, Kaluthota et al. 2015) or within family variations (Roussel et al. 2009, Marguerit et al. 2014).
Figure 1.
Stable carbon isotope composition (δ13C) and water-use efficiency at different time and spatial scales. Factors and traits involved at each change of scale are listed on a gray background. ΔB and ΔBW are total tree biomass and harvested woody biomass, respectively, and T and ET are tree transpiration (or water use) and stand evapotranspiration, respectively.
Stable carbon isotope composition (δ13C) and water-use efficiency at different time and spatial scales. Factors and traits involved at each change of scale are listed on a gray background. ΔB and ΔBW are total tree biomass and harvested woody biomass, respectively, and T and ET are tree transpiration (or water use) and stand evapotranspiration, respectively.
Hu et al. (2021) examined variations of δ13C in leaves and stems of Salix eriocephala individuals from 34 populations selected from within the large natural range of the species across eastern and western Canada. They were able to show that Wi (estimated from δ13C) varied among populations and to relate these variations to the geographical and climatic characteristics of the sites of origin. A large number of studies have shown population differences in Wi for forest trees. However, only a few of these studies have actually related these differences to the variation in environmental conditions among the original populations, thereby suggesting adaptive differences.
As Wi generally increases under drought stress, one hypothesis is that this would also be the case with respect to adaptive differences among populations, so that populations from dry environments would have a high Wi. As a first approximation, a negative correlation between the mean Wi of different populations and the precipitation of their original environments would sustain this hypothesis, which has been substantiated by a number of studies on tree species (e.g., Aitken et al. 1995, Li et al. 2000, Cregg and Zhang 2001, Bekessy et al. 2002, Zhang et al. 2005, Aleta et al. 2009).
However, this hypothesis is not necessarily the only explanation. To elaborate on an alternative hypothesis, we need to look at water-use efficiency at the whole-plant level, where it is defined as the ratio of dry biomass accumulation per unit water transpired, namely the transpiration efficiency (TE). Maximov (1929) suggested that there was no direct proportionality between TE and the degree of drought resistance, but that TE was an indicator for the ecological drought adaptation strategy of a plant. He found both high and low TE plants among different herbaceous species that were adapted to dry environments (xerophytes). He then demonstrated that plants with high TE developed rapidly and had a large leaf area, whereas plants with low TE were characterized by large root systems. Similarly, Ehleringer (1993) found high and low Wi individual plants within the species Encelia farinosa, a drought-deciduous desert shrub. He hypothesized that such plants with low Wi might allocate more carbon to the root system than those with high Wi. Recent research on Arabidopsis thaliana ecotypes has shown that different drought adaptation strategies can exist within one species, where high Wi was suggested to correspond to drought-sensitive and early closing stomata and low Wi to a drought escape strategy due to early flowering (Lovell et al. 2013, Kenney et al. 2014, Campitelli et al. 2016, Lorts and Lasky 2020). These works thus substantiate a second hypothesis, where populations from dry environments would have a low Wi. The evolution of such a strategy would result in a negative relationship between δ13C and the drought index of the populations, as reported by Hu et al. (2021). Similar results have been found for other tree species, where populations from low precipitation environments had low Wi (Nguyen-Queyrens et al. 1998) or low TE (Fan et al. 2008). But for trees, unlike annual plants, escaping drought is not an option. Therefore, drought-adapted trees with a low Wi, due to more open stomata, could either correspond to a drought tolerance strategy, for example by anatomical adaptations reducing vulnerability to cavitation, or to a drought avoidance/water spender strategy through a wide soil exploration by roots. Both strategies would allow stomata to remain open to some extent during drought. Eriksson et al. (2005) demonstrated that European Castanea sativa populations from the driest sites showed the lowest Wi, but also had the deepest rooting pattern (Lauteri et al. 2004; M. Lauteri, personal communication). This response was similar to that of low TE xerophytes in Maximov’s study and consistent with Ehleringer’s hypothesis. On the other hand, drought-adapted trees with a high Wi (the first hypothesis above) could correspond to a drought avoidance/water saving strategy, through drought-sensitive, early closing stomata.
Hu et al. (2021) included two drought indices in a canonical correlation analysis to show that Wi was more related to the duration and the temperature of the growing seasons than water availability. The use of drought indices to characterize the dryness of an environment is an improvement over the use of precipitation only, as these indices take in account other atmospheric variables. However, drought indices often do not directly reflect seasonal variation in precipitation and temperature. A generally dry climate with low but regular precipitation does not correspond to the same selection pressure as a highly seasonal climate with a strong drought (even if the overall net precipitation might be the same). The few studies that have taken into account seasonality (Voltas et al. 2008 for Pinus halepensis; Soolanayakanahally et al. 2009 for Populus balsamifera) could relate populations with a higher Wi to sites with a stronger seasonality of drought, compared with climates with less seasonal variability. In addition, the variation of soil types between environments is only rarely taken into account, even though the soil type has a strong impact on the long-term soil water availability. Raddad and Luukkanen (2006) found a higher Wi for Acacia senegal populations from sandy soils with a low water holding capacity, compared with soils with a higher clay content.
There is thus substantial evidence in the literature on forest trees, which suggests that population differences in δ13C, observed in a common environment, are linked to environmental differences in their original locations. In many cases, a higher Wi is observed for populations from drier sites, but a few examples also show a lower Wi at drier sites, supporting the interpretation of population differences in Wi as an indicator of differences in ecological strategies. To facilitate the interpretation of variations in Wi among populations in terms of adaptive strategies, a comprehensive characterization of the strength and timing of the soil water deficit seems necessary. Moreover, adaptive strategies should also be explored by analyzing the underlying functional causes of the observed diversity in Wi.
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