Spatio‐temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle

Abstract

Summary• Leaf growth dynamics are driven by diel rhythms. The analysis of spatio-temporal leaf growth patterns in Arabidopsis thaliana wild type and mutants of interest is a promising approach to elucidate molecular mechanisms controlling growth. The diel availability of carbohydrates is thought to affect diel growth.• A digital image sequence processing (DISP)-based noninvasive technique for visualizing and quantifying highly resolved spatio-temporal leaf growth was adapted for the model plant A. thaliana . Diel growth patterns were analysed for the wild type and for a mutant with altered diel carbohydrate metabolism.• A. thaliana leaves showed highest relative growth rates (RGRs) at dawn and lowest RGRs at the beginning of the night. Along the lamina, a clear basipetal gradient of growth rate distribution was found, similar to that in many other dicotyledonous species. The starch-free 1 ( stf1 ) mutant revealed changed temporal growth patterns with reduced nocturnal, and increased afternoon, growth activity.• The established DISP technique is presented as a valuable tool to detect altered temporal growth patterns in A. thaliana mutants. Endogenous changes in the diel carbohydrate availability of the starch-free mutant clearly affected its diel growth rhythms.

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).…”

“…However, when we looked at spatial maps of individual samples, we also saw much "patchier" patterns at later time points, with regions of high relative growth interspersed with regions of lower relative growth, compared with clearer gradients at the earlier time points. This patchiness has also been noted to some extent in other leaf growth analyses (Christ, 2005;Wiese et al, 2007). Christ (2005) hypothesized that this could be associated with patchy stomatal conductance, as spatial variation in stomatal openings could result in small spatial heterogeneities in turgor pressure and thus growth.…”

“…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.…”

Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins

“…In veins, aquaporins would contribute to whole rosette hydraulics (K ros ) to facilitate leaf water supply and possibly optimize growth at night or dawn (Wiese et al, 2007;Postaire et al, 2010). Consistent with this, Arabidopsis leaves show, from 4 d after emergence, hydraulically limited expansion during the day (Pantin et al, 2011).…”