Scaling of phloem hydraulic resistance in stems and leaves of the understory angiosperm shrub Illicium parviflorum

Abstract

Citation: Losada, J. M. and N. M. Holbrook. 2019. Scaling of phloem hydraulic resistance in stems and leaves of the understory angiosperm shrub Illicium parviflorum. American Journal of Botany 106(2): 244-259. PREMISE OF THE STUDY:Recent studies in canopy-dominant trees revealed axial scaling of phloem structure. However, whether this pattern is found in woody plants of the understory, the environment of most angiosperms from the ANA grade (Amborellales-Nymphaeales-Austrobaileyales), is unknown. METHODS:We used seedlings and adult plants of the understory tropical shrub Illicium parviflorum, a member of the lineage Austrobaileyales, to explore the anatomy and physiology of the phloem in their aerial parts, including changes through ontogeny.KEY RESULTS: Adult plants maintain a similar proportion of phloem tissue across stem diameters, but larger conduit dimensions and number cause the hydraulic resistance of the phloem to decrease toward the base of the plant. Small sieve plate pores resulted in an overall higher sieve tube hydraulic resistance than has been reported in other woody angiosperms. Sieve elements increase in size from minor to major leaf veins, but were shorter and narrower in petioles. The low carbon assimilation rates of seedlings and mature plants contrasted with a 3-fold higher phloem sap velocity in seedlings, suggesting that phloem transport velocity is modulated through ontogeny. CONCLUSIONS:The overall architecture of the phloem tissue in this understory angiosperm shrub scales in a manner consistent with taller trees that make up the forest canopy. Thus, the evolution of larger sieve plate pores in canopy-dominant trees may have played a key role in allowing woody angiosperms to extend beyond their understory origins.

Conductivity of the phloem inMangifera indicaL.

“…In order to avoid the fixation step, our work with mango showed that staining fresh sections for callose with aniline blue can be an unexpensive, fast, and relatively easy tool to identify the sieve tubes. The use of aniline blue to measure sieve tube element length in longitudinal fresh sections has been used in a number of cases (Savage et al ., 2017; Losada and Holbrook, 2019; Clerx et al ., 2020). However, there are few reports in which callose served to detect the sieve tubes in cross sections of woody stems, with some exceptions such as Bombax buonopozense and Sterculia tragacantha (Lawton and Canny, 1970) or the shrub Illicium parviflorum (Losada and Holbrook, 2019), where callose staining has been instrumental in the quantification of the cross sectional variation of the phloem tissue in the different axial positions along the stem.…”

“…Trees were 6 year old grafted onto polyembrionic Gomera-4 rootstock. Given that the trees are pruned to keep a manageable canopy, we sampled branches of increasing diameters, from the current year branches to the base of the trees, following the protocol previously used for shrubs (Losada and Holbrook, 2019). Thus, we selected three branches per tree oriented to all directions, and, in each branch, four diameters with increasing thickness: between 6-8mm, 13-15mm, 26-28mm and 44-46mm (Fig.1).…”

“…Trees were 6 year old grafted onto polyembrionic Gomera-4 rootstock. Given that the trees are pruned to keep a manageable canopy, we sampled branches of increasing diameters, from the current year branches to the base of the trees, following the protocol previously used for shrubs (Losada and Holbrook, 2019).…”

“…The geometrical scaling of the phloem conduits along the trunks of trees have remained unexplored until recently, when the development of microscopy techniques have allowed detailed visualization of the micro conduits of the phloem, most remarkably the quantification of the micro pores composing the sieve plates (Mullendore et al, 2010). As a result, the axial geometrical scaling of the phloem conduits in the branches of trees has been revealed in forest trees (Liesche et al, 2016;Savage et al, 2017;Clerx et al, 2020), or in the tapering branches of shrubs (Losada and Holbrook, 2019). Scaling of the conduits goes in line with the geometry of the pores, which offer most of the resistance to sap flow in the phloem, as evaluated by the most recent models of hydraulic transport (Jensen et al, 2012(Jensen et al, , 2014.…”

“…The phloem is the vascular tissue that transports photoassimilates from the source photosynthetic organs toward the sink tissues, which are the growing organs of the plant, including the roots, the meristems, fruits or the inflorescences (Esau, 1969; Heo et al ., 2014). This continuous piping system hydraulically drives substances at long and short distances, and works according to the osmotically generated pressure flow hypothesis, proposed almost a century ago (Münch, 1930), but empirically tested in a few woody organisms recently (Savage et al ., 2017; Losada and Holbrook, 2019; Clerx et al ., 2020). The hydraulic function of the phloem is intimately linked with the architecture of the individual conduits composing the tube, which are connected in series, and thus follow the laws of an electric circuit with resistances to flow (the connections between tubes or sieve plates).…”