- Top of page
- Materials and Methods
Plant respiration (R) is an integral component of the terrestrial global carbon cycle, with 30–70% of the CO2 fixed by daily photosynthesis being released by plant R (Poorter et al., 1990; Loveys et al., 2002). Globally, plant R releases c. 60 Gt C yr−1 (Schlesinger, 1997; Field, 2001); in comparison, anthropogenic CO2 releases are only c. 8 Gt C yr−1. Roots contribute 30–50% of the CO2 released by whole plant R (Poorter et al., 1990) and up to 60% of total soil CO2 efflux (Hanson et al., 2000). Alterations in rates of root R can, therefore, have profound effects on the carbon economy of individual plants, and influence CO2 exchange rates at ecosystem and global scales (Hanson et al., 2000; Gifford, 2003; Schulze, 2006).
One factor that is likely to play an important role in determining variations in specific rates of root R is a plant's mycorrhizal status. For example, formation of the arbuscular mycorrhizal (AM) symbiosis, which is characteristic of the majority of land plant species (Smith & Read, 2008), has been associated with higher rates of root R compared with nonAM plants (Baas et al., 1989; Valentine & Kleinert, 2007) and increased soil CO2 release (Langley et al., 2005). Several factors could contribute to higher rates of root R in AM-colonized plants, including increased substrate availability associated with enhanced nutrient uptake and increased demand for respiratory products (i.e. ATP, reducing equivalents and TCA cycle intermediates) (Hughes et al., 2008). For example, respiratory ATP is probably required for each of the four stages of nutrient uptake by an AM plant (i.e. ion uptake by the external fungal hyphae, ion transport within the fungus, ion export by the internal hyphae, and ion uptake by plant root cells) (Hughes et al., 2008). Increased demand for ATP is likely to decrease adenylate restriction of flux through phosphofructokinase, pyruvate kinase, the pyruvate dehydrogenase complex and the proton-translocating steps of the mitochondrial electron transport chain (Wiskich & Dry, 1985; Loef et al., 2001). It may also explain why mitochondria concentrate around the arbuscules in root cortex cells of Medicago truncatula colonized by the AM fungus Glomus intraradices (Lohse et al., 2005). However, no study has investigated whether formation of the AM symbiosis is associated with a decline in adenylate restriction, a change in the capacity of individual steps of the respiratory system associated with ATP synthesis (e.g. cytochrome c oxidase, COX) and/or overall respiratory capacity.
Temperature contributes to variations in specific rates of root R. Understanding how AM colonization impacts on the temperature response of root R is vital if global circulation models (GCMs) are to predict future rates of CO2 release by soils into the atmosphere. In most GCMs, root R is assumed to increase in a simple exponential manner in response to temperature, with a Q10 (temperature sensitivity of R; the proportional increase in respiration per 10°C increase in temperature) of 2.0 (Cox, 2001). In reality, however, the Q10 of root R is highly dynamic, with Q10 values of 1.1 to 4.6 reported (Boone et al., 1998; Tjoelker et al., 1999; Loveys et al., 2003). Variations in Q10 likely reflect shifts in the control exerted by maximum enzyme activity, substrates and/or adenylate limitations (Atkin & Tjoelker, 2003). Covey-Crump et al. (2002) found that Q10 values of root R in nonAM plants increased in response to increased substrate supply or reduced adenylate restriction. Given that formation of the AM symbiosis might increase ATP turnover (and thus reduce adenylate restriction and/or substrate supply) (Hughes et al., 2008), the short-term temperature dependence of root R may be greater in plants when colonized by AM fungi compared with those that are uncolonized. There is evidence that ectomycorrhizal (ECM) colonization alters the short-term temperature dependence of root R (Koch et al., 2007). Boone et al. (1998) concluded that the Q10 values for mycorrhizas and rhizosphere heterotrophs must be substantially greater than those of roots per se in a mixed temperate forest. By contrast, there was no evidence that Q10 values differ among mycorrhizal roots, extraradical mycelium (ERM; the external fraction of mycorrhizal hyphae in soil) and soil lacking both roots and ERM in ECM seedlings of Pinus muricata (Bååth & Wallander, 2003). Moreover, Langley et al. (2005) found that the Q10 of soil CO2 efflux was similar in AM and nonAM sunflower plants growing in pots. Thus, there is currently no consensus about whether mycorrhizal colonization alters the Q10 of root R.
Over longer time periods, the response of root R to temperature will depend on the extent of thermal acclimation. Acclimation can result in cold- and warm-grown plants exhibiting similar rates of R when measured at their respective growth temperatures (i.e. respiratory homeostasis; Larigauderie & Körner, 1995). Cold-acclimated plants also exhibit higher rates of R than their warm-grown counterparts, when R is measured at a single moderate temperature (e.g. 20–25°C). There is growing evidence that thermal acclimation of root R is common in nonAM plants (Atkin et al., 2005a and references cited therein) and that respiratory acclimation occurs in soils (reflecting CO2 release by roots, AM fungi and other heterotrophs), as shown by the response of a tallgrass prairie system to artificial warming (Luo et al., 2001). Moreover, there is some indication that some species of ECM fungi grown in axenic cultures (Malcolm et al., 2008) can acclimate to temperature. Similarly, the ERM of the AM fungus Glomus mosseae exhibited near-complete respiratory homeostasis in a soil-warming experiment (Heinemeyer et al., 2006). Although it is not known if formation of the AM symbiosis alters the degree of acclimation exhibited by root R, differences between AM and nonAM plants might be expected if the acclimation potential of the plant partner differs from that of the intraradical mycelial (IRM; i.e. AM hyphae inside the root) of the AM symbiosis. Maximal respiratory homoeostasis in roots of nonmycorrhizal plants requires the production of new tissue (Loveys et al., 2003). As the lifespan of AM fungal tissue is short (Staddon et al., 2003), rapid turnover of IRM in roots experiencing a change in growth temperature could potentially alter the extent of respiratory homeostasis.
Our study assessed the interactive effects of colonization by AM fungi and temperature on rates of root R in Plantago lanceolata. The following hypotheses were tested: (i) rates of root R are higher in AM plants than in their nonAM counterparts (i.e. same plant species with or without AM inoculum); (ii) higher rates of root R in AM plants reflect increases in substrate supply and/or demand for respiratory ATP, combined with an increase in respiratory capacity (particularly of enzymes associated with ATP production); and (iii) the Q10 and degree of thermal acclimation of R are both greater in roots of AM plants than in their nonAM counterparts.