The Plant Vascular System: Evolution, Development and FunctionsF

(Equation 1) were a major constraint over rates of phloem
translocation (Canny 1975), a notion later dispelled by the
finding that specific mass transfer rates could be elevated by
an order of magnitude in modified plant systems (Passioura
and Ashford 1974; Smith and Milburn 1980a; Kallarackal and
Milburn 1984). More recently, a quest to obtain greater insights
into sieve tube transport function (Thompson 2006) has reignited
an interest in obtaining measures of sieve tube geometries
to obtain meaningful estimates of sieve tube hydraulic
conductivities (Thompson and Wolniak 2008; Mullendore et al.
2010; Froelich et al. 2011).
On the assumption that flows through sieve tube lumens
and sieve pores are laminar, hydraulic conductivity (L) can be
derived from the Hagen-Poiseulli Law as:
L = πr 2 /8ηl (5)
A technically innovative and thorough quantitative plant
anatomical study, undertaken across a range of eudicot herbaceous
life forms, yielded estimates of sieve tube hydraulic
conductivities (Mullendore et al. 2010). Values of L were
found to be dominated by sieve pore radii, as predicted
by Equation 5, and were inversely related with independent
measures of phloem transport velocities. Such an outcome
is in contradiction to the Hagen-Poiseulli Law. Together
with other phloem transport anomalies, such as gradients
of sieve tube hydrostatic pressures not scaling with plant
size (Turgeon 2010b), these studies point to a key feature
in phloem translocation likely being overlooked. As outlined
below, we contend that sieve tube properties that establish conduits
of exceptionally high hydraulic conductivities, combined
with their ability to osmoregulate, can account for transport
phloem being capable of supporting high fluxes over long (m)
distances.
As indicated by Equation 5, sieve tube length (l), and most
importantly, sieve pore radius (r), have a direct influence on
hydraulic conductivity, along with sap viscosity (η). Sieve-tube
sap viscosity varies approximately 2.5-fold across the range
of measured sieve-tube sucrose concentrations (300 mM to
1000 mM sucrose) and, hence, could influence sieve tube
hydraulic conductivity. The viscosity of a 600 mM sucrose
solution increases approximately 2-fold from 25 ◦ C to 0 ◦ C
(Misra and Varshin 1961). A controlled experiment, in which an
approximate doubling of phloem sap viscosity can be achieved
without impacting source or sink activities, is to gradually (to
avoid shock) cool a stem zone (from 25 ◦ C to just above 0 ◦ C).
Absence of any slowing of transport rates through the cooled
zone (Wardlaw 1974; Minchin and Thorpe 1983; Peuke et al.
2006) argues that this range of phloem sap viscosities exerts
little influence over phloem transport.
To date, studies of hydraulic conductivities deduced from
sieve tube geometries have yielded ambiguous results (Mullendore
et al. 2010; Froelich et al. 2011). However, indirect
Insights into Plant Vascular Biology 327
observations suggest that sieve tube hydraulic conductivity
is unlikely to constrain phloem transport. For instance, removal
of substantial proportions of transport phloem crosssectional
area from the stem had little impact on rates of
translocation through the narrowed phloem zone (Wardlaw
and Moncur 1976), thus indicating a considerable spare capacity
for phloem transport. A spectacular example illustrating
excess transport capacity is provided by a study of translocation
rates through pedicels supporting developing apical
fruits in racemes of Ricinus. Upon removal of apical fruits,
and allowing exudation from their severed petiole stumps to
proceed, translocation rates increased from 166 g to 3111
g biomass m −2 sieve-tube area s −1 , a response suggesting
that phloem transport was sink controlled, not phloem pathway
controlled (Smith and Milburn 1980a; Kallarackal and Milburn
1984).
Experimental measurements conducted using a microfluidic
system simulating phloem pressure flow as well as transport
properties of ‘real’ plants (including tall trees) also yielded
results that conformed with predictions of the Münch model
(Jensen et al. 2011, 2012). Studies performed on an Arabidopsis
mutant lacking P-protein agglomerations in sieve tubes, and
hence conferring higher sieve tube conductivity, established
that these plants had similar transport velocities (or volume
flux – see Equation 2) to WT plants (Froelich et al. 2011).
Collectively, these studies support the notion that sieve-tube
hydraulic conductivities do not impose a significant limitation
on transport fluxes along phloem pathways, even over considerable
lengths of sieve tubes. Rather, as discussed above, the
majority of control may well be exercised by bulk flow through
PD linking SE-CC complexes of release phloem with adjacent
phloem parenchyma cells (Figure 13C).
Pressure-concentration waves generated by phloem unloading
are transmitted over considerable distances (m) at velocities
an order of magnitude higher than those of phloem translocation
(Smith and Milburn 1980a; Mencuccini and Hölttä 2010).
Such a signaling system is envisioned to underpin unified
responses by all SE-CC complexes, comprising phloem paths
from release to collection phloem, to altered resource demands
by the various sinks (Thompson 2006). These responses are
mediated by turgor-regulated membrane transport of sugars
into SE-CC complexes; these sugars are supplied from mesophyll
and axial pools for compensation within collection and
transport phloem, respectively (Figure 13A). This mechanism
results in homeostasis of hydrostatic pressure in sieve tubes
along the phloem pathway (Gould et al. 2004a). The action
of this pressure-concentration signaling system could account
for differentials in hydrostatic pressures between collection and
release phloem not scaling with transport distance, particularly
in tall trees (Turgeon 2010b). In addition, such a mechanism
could maintain sieve-tube sap concentrations of all solutes
(Gould et al 2004a) and, hence, their rates of phloem transport.