In leaves of higher plants, the processes of respiratory CO2 release (R) and photosynthetic CO2 uptake (P) are interdependent. On the one hand, R relies on P substrates, while on the other, P is dependent on R for the carbon skeletons and for the ATP required for sucrose synthesis plus repair of photosynthetic proteins (Krömer, 1995; Hoefnagel et al., 1998; Padmasree et al., 2002). As a result, the instantaneous R/P ratio in individual leaves is often constant, even in plants experiencing contrasting growth temperatures (Gifford, 1995; Ziska & Bunce, 1998; Dewar et al., 1999; Loveys et al., 2003; Atkin et al., 2006). This constancy, if held over extended periods, raises the possibility that global carbon cycle models can assume homeostasis of R/P when predicting future CO2 fluxes between plants and the atmosphere (Gifford, 2003). However, such an assumption requires that R/P be homeostatic not only in individual leaves but also in whole plants.
In whole plants, several factors can contribute to differences in R/P compared with that observed in individual mature leaves. Firstly, stem and root R values contribute to daily respiratory CO2 release in whole plants; because of this, R/P is greater in whole plants than in individual leaves. Secondly, irradiances experienced by whole shoots are often not saturating or uniform throughout the canopy; as a result, rates of light-saturated P in leaves are often a poor indicator of P in whole shoots (e.g. Evans et al., 2000). Thirdly, in whole plants, mature and immature tissues both contribute to CO2 exchange. Young tissues respire at higher rates (Collier & Grodzinski, 1996; Radoglou & Teskey, 1997; Millar et al., 1998; Oleksyn et al., 2000; Armstrong et al., 2006) than mature tissues and maximal rates of P are not exhibited until leaves are fully expanded (Evans et al., 2000; Miyazawa & Terashima, 2001). As a result, the presence of young tissues in whole plants can alter R/P ratios.
Because P and R are temperature sensitive, a change in temperature results in an immediate alteration in the rate of R and P, with the extent of that alteration being determined by the temperature coefficient of each process. The temperature sensitivity of P differs from that of R, with the result that R/P is altered following a short-term (i.e. minutes to hours) change in measuring temperature (Dewar et al., 1999; Hansen et al., 2002; Gifford, 2003; Atkin et al., 2006). However, in many species, homeostasis of R/P in individual leaves is re-established when plants experience contrasting temperatures for sustained periods (i.e. as a result of thermal acclimation of specific rates of R and P; Loveys et al., 2003; Tjoelker et al., 1999a). Given that the degree to which specific rates of R and P acclimate differs among species (Berry & Björkman, 1980; Larigauderie & Körner, 1995; Tjoelker et al., 1998, 1999b; Xiong et al., 1999, 2000; Loveys et al., 2002; Atkin et al., 2006), and among different tissues within individual plants (Atkin et al., 2005; Armstrong et al., 2006), it seems unlikely that all species will exhibit the same degree of homeostasis of whole-plant R/P when grown under contrasting temperatures.
In contrast to the growing number of studies that have investigated the effect of growth temperature on R/P of individual mature leaves, relatively few studies have investigated the impact of growth temperature on R/P in whole plants using actual measurements of whole-plant gas exchange. Gifford (1995) found that daily R/P was constant for potted-grown wheat (Triticum aestivum) developed at constant temperatures ranging from 15 to 30°C. Similarly, soybean (Glycine max) grown at a range of growth temperatures between 20 and 35°C showed no differences in R/P (Ziska & Bunce, 1998). However, in the latter study, growth under an elevated concentration of CO2 (700 µl l−1) did result in reduced R/P, compared with growth at ambient CO2 (350 µl l−1). Similarly, Loveys et al. (2002) found that plants grown at 28°C exhibited higher whole-plant R/P ratios than did the plants grown at 18 and 23°C. The extent to which whole-plant R/P values remain homeostatic under contrasting growth temperatures therefore appears to be variable.
A factor that could contribute to temperature-mediated changes in R/P is the impact of growth temperature on biomass allocation to roots, stems and leaves. When considered alone, increased allocation to roots would lead to an increase in whole-plant R/P (as a result, in part, of an increase in overall respiratory carbon release by roots, whose specific rates of R are typically higher than those of stems and leaves). Where increased investment in roots is associated with a decrease in biomass allocation to leaves, reductions in shoot P would further exacerbate increases in R/P. There is evidence that growth at low temperatures can result in increased allocation of biomass to roots in some species (Equiza & Tognetti, 2002), whereas in other species the effect of temperature on root biomass is variable depending on the growth temperatures being compared (DeLucia et al., 1992). To our knowledge, no study has previously established the role temperature-mediated changes in biomass allocation play in determining the whole-plant R/P values.
The objective of our study was to investigate the impact of sustained differences in growth temperature, and short-term changes in air temperature, on the whole-plant carbon economy of two congeneric Plantago species from contrasting habitats. The lowland Plantago major and the alpine Plantago euryphylla differ in maximum relative growth rate (RGR; Loveys et al., 2002) and in their ability to thermally acclimate specific rates of leaf P and R (Atkin et al., 2006). What is not known, however, is whether differences in the ability to acclimate leaf metabolism are associated with differences in acclimation of P and R and/or homeostasis of R/P at the whole-plant level. By measuring CO2 exchange in shoots separately from that of roots, we were able to obtain accurate estimates of the temperature dependence of intact shoot and root R, and shoot P. We addressed the following questions. (1) To what extent is homeostasis of whole-plant R/P achieved across a range of growth temperatures in contrasting plant species differing in their ability to thermally acclimate R and P in individual leaves? (2) What role do temperature-mediated changes in biomass allocation and specific rates of R and P play in determining the ratio of R/P in whole plants? (3) To what extent do short-term variations in temperature alter whole-plant R/P values?