Phloem Loading through Plasmodesmata: A Biophysical Analysis

Abstract

In many species, Suc en route out of the leaf migrates from photosynthetically active mesophyll cells into the phloem down its concentration gradient via plasmodesmata, i.e. symplastically. In some of these plants, the process is entirely passive, but in others phloem Suc is actively converted into larger sugars, raffinose and stachyose, and segregated (trapped), thus raising total phloem sugar concentration to a level higher than in the mesophyll. Questions remain regarding the mechanisms and selective advantages conferred by both of these symplastic-loading processes. Here, we present an integrated model-including local and global transport and kinetics of polymerization-for passive and active symplastic loading. We also propose a physical model of transport through the plasmodesmata. With these models, we predict that (1) relative to passive loading, polymerization of Suc in the phloem, even in the absence of segregation, lowers the sugar content in the leaf required to achieve a given export rate and accelerates export for a given concentration of Suc in the mesophyll and (2) segregation of oligomers and the inverted gradient of total sugar content can be achieved for physiologically reasonable parameter values, but even higher export rates can be accessed in scenarios in which polymers are allowed to diffuse back into the mesophyll. We discuss these predictions in relation to further studies aimed at the clarification of loading mechanisms, fitness of active and passive symplastic loading, and potential targets for engineering improved rates of export.

Computational tools for serial block EM reveal differences in plasmodesmata distributions and wall environments

“…We performed this in part with the aim of informing future models of flow across PD with relevant experimental data. Published modelling approaches have so far studied PD transport in relation to the overall single pore structure (Blake, 1978), phloem flow (Jensen et al, 2012), phloem loading mechanisms (Comtet et al, 2017) and unloading flow type (Ross-Elliott et al, 2017). One modelling study tried to address some complexities of PD, integrating ultrastructure parameters for the cytoplasmic sleeve in their models (Liesche and Schultz 2013).…”

Phloem structure and development in Illicium parviflorum, a basal angiosperm shrub

“…As a member of the basal grade of flowering plants, Illicium could likely fit with the previously hypothesized passive sugar loading in woody angiosperms of the understory (Gamalei, 1989; 1991). However, this feature appears to be labile among the extant members of the basal angiosperm grade, such as the active loading reported for Amborella (Turgeon & Medville, 2011; Comtet et al ., 2017).…”

From plasmodesma geometry to effective symplasmic permeability through biophysical modelling

“…Small molecules can move via PD by diffusion (non-targeted transport). This is considered to be predominantly symmetrical ( Schönknecht et al, 2008 ; Maule, 2008 ), while in certain tissues, such as secreting trichomes ( Waigmann and Zambryski, 1995 ; Gunning and Hughes, 1976 ) and the phloem ( Ross-Elliott et al, 2017 ; Comtet et al, 2017 ), hydrodynamic flow may create directionality. The maximum size of molecules that can move by this generic “passive” pathway is often referred to as the “size exclusion limit” (SEL), which obviously depends on PD properties and structural features ( Dashevskaya et al, 2008 ).…”

“…Computational modelling approaches have been applied to model PD transport but, so far, these have mainly focused on hydrodynamic flow and the specific tissues where that matters ( Blake, 1978 ; Bret-Harte and Silk, 1994 ; Jensen et al, 2012 ; Ross-Elliott et al, 2017 ; Comtet et al, 2017 ; Foster and Miklavcic, 2017 ; Couvreur et al, 2018 ). The few existing studies on diffusive transport do not consider neck constrictions or the approach to PDs from the cytoplasmic bulk.…”

“… Ross-Elliott et al ( 2017 ) also consider “funnel” shaped PDs, which are observed in the phloem unloading zone, but ignore the DT in their diffusion model, as they only calculate a best case scenario for diffusive transport. In the context of size selectivity for small (sugar) molecules in phloem loading, also the so-called “sub-nano channel model” of PD geometry has been considered ( Liesche and Schulz, 2013 ; Comtet et al, 2017 ). In this model, symplasmic transport is modelled to be confined to nine cylindrical channels spanning the PD.…”