Spatial and Temporal Effects of Free-Air CO2Enrichment (POPFACE) on Leaf Growth, Cell Expansion, and Cell Production in a Closed Canopy of Poplar

Abstract

Leaf expansion in the fast-growing tree, Populus ϫ euramericana was stimulated by elevated [CO 2 ] in a closed-canopy forest plantation, exposed using a free air CO 2 enrichment technique enabling long-term experimentation in field conditions. The effects of elevated [CO 2 ] over time were characterized and related to the leaf plastochron index (LPI), and showed that leaf expansion was stimulated at very early (LPI, 0-3) and late (LPI, 6-8) stages in development. Early and late effects of elevated [CO 2 ] were largely the result of increased cell expansion and increased cell production, respectively. Spatial effects of elevated [CO 2 ] were also marked and increased final leaf size resulted from an effect on leaf area, but not leaf length, demonstrating changed leaf shape in response to [CO 2 ]. Leaves exhibited a basipetal gradient of leaf development, investigated by defining seven interveinal areas, with growth ceasing first at the leaf tip. Interestingly, and in contrast to other reports, no spatial differences in epidermal cell size were apparent across the lamina, whereas a clear basipetal gradient in cell production rate was found. These data suggest that the rate and timing of cell production was more important in determining leaf shape, given the constant cell size across the leaf lamina. The effect of elevated [CO 2 ] imposed on this developmental gradient suggested that leaf cell production continued longer in elevated [CO 2 ] and that basal increases in cell production rate were also more important than altered cell expansion for increased final leaf size and altered leaf shape in elevated [CO 2 ].Given the importance of forests for global bioproductivity, the consequences of increased atmospheric [CO 2 ] for the global carbon cycle are potentially extremely large (Malhi et al., 1999). Despite this, there are still relatively few large-scale, long-term experiments from which predictions about likely forest responses can be made. Few studies have been completed where trees are allowed to develop to canopy closure and where a "stable" response to [CO 2 ] is likely. Determining the response of leaf area development to elevated [CO 2 ] is important. It is still unknown whether forests of the future will maintain a higher leaf area index (LAI), as implied from smalltree studies (Ceulemans et al., 1997) or whether the long-term (decades) responses will be reduced allocation to foliage and lower LAI, as suggested by some modeling approaches (Medlyn and Dewar, 1996) or involve acclimation to limited nitrogen (Oren et al., 2001).Leaf growth is often stimulated in short-term response to elevated [CO 2 ] (Taylor et al., 1994;Pritchard et al., 1999), and both leaf cell expansion and cell production are sensitive to [CO 2 ] (Taylor et al., 1994). It is likely that these processes respond to additional carbohydrate from photosynthesis and, as such, altered atmospheric [CO 2 ] provides a critical insight into how carbon regulates plant development and growth (Masle, 2000). The importance of leaf develo...

Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions

“…Moreover, the growth patterns we observed are consistent with other leaf growth analyses, which have shown a similar proximodistal gradient in growth rates in Arabidopsis (Wiese et al, 2007) as well as in other species, such as tobacco (Nicotiana tabacum; Avery, 1933;Poethig and Sussex, 1985;Walter and Schurr, 1999;Walter et al, 2003), sunflower (Helianthus annuus; Granier and Tardieu, 1998), grape (Vitis vinifera; Wolf et al, 1986), spinach (Spinacia oleracea; Saurer and Possingham, 1970), cocklebur (Xanthium pensylvanicum; Maksymowych, 1959;Erickson, 1966), ivy (Hedera helix; Wang et al, 2011), and poplar (Populus spp. ; Taylor et al, 2003). An exception to this pattern was shown in soybean (Glycine max; Ainsworth et al, 2005), where no spatial gradient was observed, leading the authors to conclude that the mechanisms of leaf growth in soybean may be different from that in other species.…”

“…Early efforts to measure leaf growth involved drawing ink dots on the adaxial leaf surface to delineate a grid of small rectangles whose deformations over time could be used to calculate regional growth rates (Avery, 1933;Richards and Kavanagh, 1943). Other studies since then have employed the same concept of quantifying growth at the adaxial leaf surface by tracking ink marks (Maksymowych, 1962;Saurer and Possingham, 1970;Poethig and Sussex, 1985;Granier and Tardieu, 1998;Wang et al, 2011) or vein intersections (Maksymowych, 1959;Erickson, 1966;Wolf et al, 1986;Walter and Schurr, 1999;Taylor et al, 2003;Walter et al, 2003). Recently, digital image sequence analysis tools have been developed to automatically track the displacement of identifiable features in successive images of a leaf (Schmundt et al, 1998;Ainsworth et al, 2005;Wiese et al, 2007).…”

“…This is because drawing or printing ink dots on the leaf surface (Avery, 1933;Richards and Kavanagh, 1943;Maksymowych, 1962;Poethig and Sussex, 1985;Granier and Tardieu, 1998;Wang et al, 2011) or threading or clipping weights through the leaf margins, as required for the digital image sequence analysis setup (Schmundt et al, 1998;Ainsworth et al, 2005;Wiese et al, 2007), require that the leaf be relatively large, and vascular features (Maksymowych, 1959;Erickson, 1966;Wolf et al, 1986;Walter and Schurr, 1999;Taylor et al, 2003;Walter et al, 2003) are not visible at early stages of development.…”

The Effects of Elevated CO2 Concentration on Soybean Gene Expression. An Analysis of Growing and Mature Leaves

“…Increased leaf growth, leading to larger individual leaf size, is one component of increased LAI measured at elevated [CO 2 ] in field experiments (Taylor et al, 2003;Tricker et al, 2004;Dermody et al, 2006). At the molecular level, the basis for changes in LAI at elevated [CO 2 ] is largely unknown.…”

“…At the molecular level, the basis for changes in LAI at elevated [CO 2 ] is largely unknown. Both cell production rates and cell expansion have been shown to be sensitive to elevated [CO 2 ] (Taylor et al, 1994(Taylor et al, , 2003. Transcript analysis of growing poplar (Populus spp.)…”