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- Materials and Methods
- Supporting Information
Current distributions of plant species reflect evolutionary adaptation to a variety of environmental factors. Amongst these, temperature and precipitation are pre-eminent in defining the climate of a region, and together with characters such as soil moisture retention define the duration of growth periods for plants. Geographic patterns of plant growth and productivity reflect the climate under which plant communities evolved (Schlesinger, 1997; Schulze et al., 2002). For instance, plant development requires favourable temperature conditions and therefore proceeds in accordance with thermal time (i.e. the classical temperature-sum concept of plant development; Thornley & Johnson, 1990; Granier et al., 2002). At high latitudes and/or in alpine areas, the time suitable for plant development varies with altitude, as does the species composition of plant communities (von Humboldt, 1845).
In alpine areas, plants not only have to cope with low average growth temperatures (or short thermal time), but also have to cope with comparatively large temporal temperature fluctuations. These recurrent and persistent patterns form the basis for adaptation of plant metabolism to climate (sensuCriddle et al., 2005; Lambers et al., 2008). We know that highland and lowland species differ in phenology (Mooney, 1963; Friend & Woodward, 1990), and it is widely presumed that such differences are reflected in adaptation of physiological traits, driving plant development and growth. Rates of growth generally co-vary with rates of respiration, but it remains difficult to distinguish between respiratory acclimation to seasonal or daily temperature variation and adaptation of metabolism to prevailing climate.
Studies over many decades suggest that plant respiration (defined as rate of release of CO2 per unit plant mass, unless otherwise stated) acclimates quickly to growth temperature (Rook, 1969; Collier & Cummins, 1990; Atkin et al., 2000; Lee et al., 2005; Campbell et al., 2007). Acclimation within days to weeks of a shift in temperature can result in respiration rates remaining similar at each growth temperature (provided they are measured at the respective growth temperature). Newly developed tissues seemingly display a ‘memory’ of temperatures experienced during development, providing a significant component of the seasonal acclimation of plant metabolism. For example, plants that develop under colder conditions have greater mitochondrial density (and/or increased leaf protein contents; Klikoff, 1966; Stitt & Hurry, 2002), and cold-developed mitochondria often show changes in ultrastructure (Armstrong et al., 2006b). Enhanced capacity for respiration helps underpin required rates of anabolic and catabolic reactions (i.e. Billings et al., 1971) as, under cold conditions, the maximum velocities (vmax) of these processes are heavily dependent on the total amount of enzymes present (Kruse et al., 2011). Homeostatic responses to cold temperatures have been widely interpreted as a means of maintaining rates of metabolism under adverse conditions (Amthor, 2000). Near-neighbour competition is common in early stages of vegetative growth and individual seedlings or plantlets may need to maximize rates of growth (in competition for light), if they are to survive (Grime, 1977). By contrast, if growth at the seedling stage is ‘maximized’ at high temperatures, plants may be at risk of carbohydrate starvation (Friend & Woodward, 1990; Way & Oren, 2010). We recently suggested (Kruse et al., 2011) that acclimation of respiration to seasonal, and even short-term fluctuations of temperature, might thus reflect plant species’ ability to stabilize rates of growth and development according to climate. In fact, growth rates of any given plant species are surprisingly constant across a wide range of growth temperatures (Atkin et al., 2006). Respiratory acclimation can be viewed as the cumulative effects or ‘memory’ of environmental conditions during development. Acclimation of this type ensures optimization of growth and maintenance processes such that plants avoid substrate depletion. Further, and on the basis that long-term average temperature is a primary driver of rates of growth, acclimation of metabolism is a mechanism that helps compensate for deviations from such average temperatures. It is presently not known if species that are adapted to short vegetation period (or low average temperature) differ in respiratory plasticity, that is, their ability to metabolically acclimate to temperature fluctuations. Such an analysis is complicated by additional factors that determine relative growth rates (RGRs; the increase in plant mass per unit starting mass and time).
RGR can be defined as a function of net assimilation rate (NAR; the increase in plant mass per unit leaf area and time), Specific leaf area (SLA; leaf area per unit mass) and biomass allocation (leaf mass ratio (LMR); leaf mass per unit plant mass) (Lambers & Poorter, 2004; Atkin et al., 2006):
- (Eqn 1)
The term NAR can be expressed as the difference between daily, leaf area-based net photosynthesis and respiration, divided by plant carbon concentrations – as affected by storage and remobilization processes (Atkin et al., 2006). While NAR is driven by growth processes subject to short-term stabilization, changes in leaf architecture and biomass allocation are more important for regulation of plant growth in the mid and long term.
In relation to acclimation of short-term processes relevant to NAR, Tjoelker et al. (1999) found a close correlation between RGR and rates of respiration in evergreen and broad-leafed seedlings. Evergreen species showed a greater degree of respiratory acclimation than deciduous species (Tjoelker et al., 1999). Physiological plasticity apparently played a greater role in the ‘stabilized’ development of evergreen perennials than plasticity of leaf structure and biomass allocation (also see Bruhn et al., 2007 for a study with Eucalyptus spp.). Evergreen species generally display lower SLA values than deciduous species, and slow-growing herbaceous species have lower SLA values than fast-growing species (Poorter et al., 2009). The slow growth of some alpine herbaceous species seems mostly a result of lower SLA when compared with lowland species (e.g. Atkin et al., 1996), and growth and respiration are not necessarily correlated (e.g. Atkin & Day, 1990). Larigauderie & Körner (1995) found no systematic differences in the extent of respiratory acclimation to contrasting growth temperatures between lowland and alpine herbaceous species.
Large species-specific differences might be best related to different growth and life strategies. Some species control rates of growth primarily through acclimation of metabolism (i.e. Arnone & Körner, 1997), while others swiftly adjust structural traits. For example, plasticity of SLA is different in tropical and boreal species, and changes in SLA for a given change in temperature are larger in tropical species (Poorter et al., 2009). As another example, Loveys et al. (2002) demonstrated varied importance of physiological and morphological traits (particularly SLA) to differences in RGRs among species. The importance of those traits also varied among growth temperatures. For slow-growing species at moderately cold temperatures (18°C), variations in growth rates were better explained by variations in NAR than variation in SLA. Put differently, slow-growing species exhibited stronger acclimation of area-based respiration to temperature than fast-growing species (Loveys et al., 2002). This conclusion could not be confirmed in a subsequent study of mature leaves (Loveys et al., 2003) and, to reconcile the difference between studies, Loveys et al. (2003) proposed that the degree of acclimation of developing leaves may well differ from that of mature leaves. This hypothesis was confirmed for Arabidopsis by Armstrong et al. (2006a).
In the present study, we investigated physiological acclimation in young Eucalyptus seedlings, and explored variation in acclimation linked to adaptive differences between species. We studied 12 evergreen Eucalyptus species that are adapted to low, mid and high altitudes. Seedlings from each of these species were grown at four sites, along an altitude gradient in the Australian Alps. Physiological acclimation of young, developing foliage (e.g. < 1 cm2) is seldom determined because of the physical constraints of conventional CO2-exchange systems. Micro-calorimetric methods provide an excellent means of analysing small, but vigorously respiring and actively growing tissue and of simultaneously determining rates of CO2 release and O2 reduction. In the present study, we confined respiration measurements to small, newly emerged foliage. That is, respiratory acclimation was not confounded by adjustment of leaf structural traits at this early stage of development. Instantaneous rates of growth (or ‘enthalpic growth’) can be readily determined (on a per unit mass basis), as can the temperature response of respiration (Criddle et al., 1997, 2000). We show how a new parameter derived from the temperature response of instantaneous growth rates, the instantaneous growth capacity of young foliage, provides a useful tool for separating acclimation and adaptation of plant metabolism to temperature. This parameter helps to describe principal relationships between respiration and growth and helps to test the hypothesis that respiratory acclimation is a consequence of growth regulation. Further, we sought to understand the mechanistic basis for increased fitness of Eucalyptus species that are adapted to differing thermal environments.