4.2 Vascular scaling in leaves of Austrobaileyales and other angiosperms
Within leaves of A. scandens , the geometry of vascular elements (tracheids and sieve tube elements) vary across vein orders. Hierarchical scaling of the xylem has been documented in the reticulate leaves of angiosperms, suggesting that the efficiency of water distribution across the continuous xylem conduits follows laws of energy conservation, such as Murray´s law (Murray, 1926; McCulloh et al., 2003; Carvalho et al., 2017a, Scoffoni et al., 2017). In contrast, the scaling of sieve tube elements in leaf veins of woody plants remains poorly characterized. Recent work in leaves with different branching patterns, such as the dichotomously branched veins of Ginkgo (Carvalho et al., 2017b), or reticulate-veined leaves of Populus andIllicium (Carvalho et al., 2017a; Losada & Holbrook, 2019), strongly suggest universal variation of the geometry of phloem conduits across leaf vein orders. Yet, an unexplored feature in the leaves of angiosperms is the size of pores connecting sieve tubes in the leaves. Our work provides evidence that pore sizes vary in accordance with sieve tube dimensions, from 0.08µm in minor veins to 0.12µm in the petiole. As a result, variation of both the geometry of tubes and size of pores enhance bulk export of photoassimilates toward the petiole under the pressure-flow predictions (Münch, 1930).
We further report a 1:1.25 xylem to phloem ratio of areas of the major vein in Austrobaileya leaves, balanced in favor of the phloem compared to the general range of 1:4 to 1:10 reported in leaves of deciduous trees (Artschwager, 1926; Waisel et al., 1966). Additionally, the isodiametric sieve tube elements in the midrib linearly increased in number toward the petiole. The dimensions of sieve elements in the major leaf veins remains poorly explored in angiosperms, but they are well documented in the single veined needles of conifers (Ronellenfitsch et al., 2015), in which photo assimilate export is favored by the increasing number of isodiametric phloem conduits from the tip to the base of the needles. This suggests a convergent strategy between conifer needles and A. scandens midrib, but whether this is well-maintained in other angiosperm leaves, needs further testing. Furthermore, the isodiametric tracheids of the midrib linearly increased in number toward the petiole, supporting predictions on the uniformity of xylem conduit diameter within the same vein order (McCulloh et al., 2003, 2009; Gleason et al., 2018). Among the scarce studies documenting xylem allometry in single veins, variation in conduit diameter along the midrib has been studied in Fraxinus (Petit et al., 2016) andAcer (Lechthaler et al., 2019). The shortening of tracheids toward the petiole of A. scandens suggests that conductivity of water uptake by leaves is lower, in sharp contrast with the highly conductive stems, pointing to hydraulic segmentation of the xylem between the stems and the leaves. In contrast, the sieve tube elements of the petiole reduced their length, but not their diameter, thus maintaining a stable transport capacity. We previously showed a similar trait in the leaves of Illicium parviflorum (Losada & Holbrook, 2019; Carvalho et al., 2018), a pattern confirmed in leaves of five tree species: Acer saccharum , Liriodendron tulipifera ,Catalpa speciosa , Liquidambar styraciflua , andQuercus rubra (unpublished).
The special characteristics of the petioles have been previously put forward in a number of species such as in the genera Beta (Geiger et al, 1969), Cyclamen (Grimm et al., 1997), orPelargonium (Ray & Jones, 2018), suggesting architectural plasticity that is uncoupled from the leaf lamina. Strikingly, we found that the petiole of A. scandens is fiberless, in sharp contrast with the massive presence of perivascular fibers in the leaf lamina. Fiberless petioles were further observed in Illicium parviflorum(Losada & Holbrook, 2019), and suggest that these short petioles require flexibility, especially in understory plants such as the majority of members of the Austrobaileyales, which need to orientate their leaves toward sun flecks. In addition, the petioles ofA. scandens may aid with twining, as previously suggested (Feild et al., 2003b), in agreement with previous evidence of a pivotal role of petiole reorientation in generating the squeezing force that stabilize twining stems (Isnard et al., 2009).