Atmospheric CO2 concentration ([CO2]) has risen by ~30% in the last 250 yr, and data from monitoring stations, together with historical records extracted from ice cores, show that atmospheric [CO2] is now at a level higher than at any time in the last 650 000 yr (Meehl et al., 2007). Driven by the addition of 6–8 Pg carbon yr−1 from anthropogenic sources, atmospheric [CO2] is predicted to continue to rise by an additional 50% by 2050 (Meehl et al., 2007). The Intergovernmental Panel on Climate Change (IPCC) estimates that between 46 and 56% of terrestrial carbon stocks are found in forest biomes, and that actions to preserve and enhance this carbon sink would probably increase the global terrestrial carbon stock by 60–87 Pg carbon by 2050, thereby offsetting c. 15% of the anthropogenic emissions predicted for the same period (Prentice, 2001; Brown, 2002).
Aggressive afforestation is part of the action required to meet this potential for increasing the terrestrial carbon stock, and managed plantations of highly productive tree species, such as members of the genus Populus, are an attractive system to help achieve this goal (Deckmyn et al., 2004; Perlack et al., 2005). Recent advances in poplar genomic resources include the collections of over 410 000 expressed sequence tags (ESTs) in GenBank (http://www.ncbi.nlm.nih.gov/dbEST/), the development of cDNA and whole-genome microarrays (Déjardin et al., 2004; Broschéet al., 2005; Rinaldi et al., 2007) and the full genome sequence available from P. trichocarpa (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home; Tuskan et al., 2006). These advances have promoted the idea that poplar species hold great potential to be bred or engineered for an increased suitability for carbon sequestration (Sims et al., 2006).
Plants, including trees, sense and respond to increasing [CO2] through increased photosynthesis and reduced stomatal conductance (Ainsworth & Rogers, 2007; Hyvönen et al., 2007; Liberloo et al., 2007; Riikonen et al., 2008; Taylor et al., 2008). All other effects of elevated [CO2] (e[CO2]) on plants and ecosystems are derived from these two fundamental responses. However, genetic and environmental bottlenecks can determine both the magnitude of these primary responses to e[CO2] and the capacity to assimilate carbon into increased above-ground biomass (Karnosky et al., 2005; Liberloo et al., 2006; Luo et al., 2006, 2008; Ainsworth & Rogers, 2007). In trees, growth is dependent on the internal balance between carbon and nitrogen, and this balance depends not only on nitrogen resources directly available from soil and internal sources, but also on nitrogen resources from seasonal storage pools in bark, wood and roots (Luo et al., 2008). A few studies have explored the transcriptomics of individual tree species as they respond to e[CO2] (Gupta et al., 2005; Taylor et al., 2005; Druart et al., 2006). Each study identified relatively few transcriptional changes in response to e[CO2], and the results between species were quite variable, making it difficult to draw solid conclusions. Although the responses of photosynthesis, growth and biomass accumulation in trees grown at e[CO2] are well documented (Nowak et al., 2004; Ainsworth & Long, 2005; Norby et al., 2005; Ainsworth & Rogers, 2007), the molecular mechanisms that determine how different tree species achieve a balance between carbon and nitrogen assimilation, storage and eventual growth remain largely unknown. Consequently, there is a need to increase our understanding of metabolic/physiological processes that may limit the response of trees to increasing [CO2].
Free-air CO2 enrichment (FACE) provides a realistic platform on which to investigate the response of trees to e[CO2] (Long et al., 2004) and, with particular reference to this study, avoids artificial restriction of sink capacity, canopy development and nutrient supply. In this study, we have taken advantage of an ongoing FACE experiment located near Rhinelander, WI, USA (Karnosky & Pregitzer, 2006), referred to as the Aspen FACE site (http://aspenface.mtu.edu/). Here, five distinct genotypes of quaking aspen (Populus tremuloides) have been grown at e[CO2] (ambient plus 200 ppb) since 1997.
Poplar trees growing under e[CO2] generally have a larger leaf size (Oksanen et al., 2001; Riikonen et al., 2008), increased stem and branch growth (Isebrands et al., 2001; Karnosky et al., 2005; King et al., 2005; Kubiske et al., 2007) and increased root biomass (King et al., 2001; Lukac et al., 2003). However, at Aspen FACE, CO2 responsiveness was found to be genotype dependent. Clone 271 is highly responsive to e[CO2], whereas the growth of clone 216 is not significantly stimulated by e[CO2], despite the fact that both clones show similar increases in photosynthetic rates under e[CO2] (Noormets et al., 2001b; Riikonen et al., 2008; Taylor et al., 2008). Clone 271 has delayed senescence and develops ~50% more stem biomass than clone 216 in response to e[CO2] (Table 1) (Karnosky et al., 2005; Kubiske et al., 2007). By focusing on the tissues that most directly sense and respond to e[CO2], this paper provides an initial examination of the abundance of leaf gene transcripts and biochemical responses in growth-responsive (clone 271) and growth-unresponsive (clone 216) genotypes of P. tremuloides grown at ambient and e[CO2]. It is hypothesized that such an analysis of clones with markedly different growth responses to e[CO2] will allow us to identify some of the genetic trends associated with a sustained utilization of an increased carbon supply and a superior capacity for above-ground biomass production. To our knowledge, this is the first study to directly compare the leaf transcriptomes of tree genotypes of the same species having similar carbon uptake, but very different growth responses when grown at e[CO2] in the field.
|Clone 216 response to e[CO2]||Clone 271 response to e[CO2]||Reference(s)|
|Photosynthesis||+++||+++||Noormets et al. (2001b); Riikonen et al. (2008); Taylor et al. (2008)|
|Chlorophyll content||−−−||−−−||Wustman et al. (2001)|
|Rubisco||−−||ns||Wustman et al. (2001)|
|Stomatal conductance||−−||−−||Noormets et al. (2001a); Riikonen et al. (2008)|
|Stomatal frequency||ns||ns||Karnosky et al. (2003); Mankovska et al. (2005)|
|Leaf area index (LAI)||++||++||Karnosky et al. (2005) Riikonen et al. (2008); Taylor et al. (2008)|
|Leaf thickness||++||++||Oksanen et al. (2001, 2003)|
|Leaf cell wall thickness||ns||−−||Oksanen et al. (2003)|
|Leaf surface waxes||ns||++||Karnosky et al. (2002); Mankovska et al. (2005)|
|Leaf isoprene emissions||ns||ns||Calfapietra et al. (2007)|
|Leaf cytoplasmic lipids||++||+||Oksanen et al. (2001)|
|Leaf starch content||++||++||Kopper & Lindroth (2003)|
|Leaf total nitrogen||−−||−−||Kopper & Lindroth (2003)|
|Rust occurrence||+||ns||Karnosky et al. (2002); Mankovska et al. (2005)|
|Tent caterpillar performance||ns||−−||Kopper & Lindroth (2003)|
|Delayed autumn senescence||+||++||Riikonen et al. (2008); Taylor et al. (2008)|
|Diameter growth||+||+++||Isebrands et al. (2001); Kubiske et al. (2007)|
|Volume growth||+||+++||Karnosky et al. (2005); Kubiske et al. (2007)|
|Height growth||ns||+++||Isebrands et al. (2001); Kubiske et al. (2007)|
|Cell wall percentage||+||ns||Kaakinen et al. (2004)|
|Wood starch content||ns||+||Kaakinen et al. (2004)|
|Wood total nitrogen||−||−−||Kaakinen et al. (2004)|