The Plant Vascular System: Evolution, Development and FunctionsF

Other layers of post-translational control of sucrose transporter
activity include protein-protein interactions, e.g., SUT1-
SUT4 regulation of phloem loading (Chincinska et al. 2008),
redox-induced dimerization of SUT1 (Krügel et al. 2008), and
cytochrome b5 interaction with MdSUT1 and MdSOT6 (Fan
et al. 2009). Interestingly, the question as to whether symplasmic
loading species also have the capacity for short-term
adjustments in phloem loading capacity is less certain (Amiard
et al. 2005).
Magnetic resonance imaging studies, conducted on longdistance
transport of water through the vascular system in
a range of species, have established that phloem transport
remains unaffected by diurnal variations in transpiration-driven
changes in apoplasmic leaf water potential (Windt et al. 2006).
Thus, a regulatory mechanism must operate to maintain a
constant pressure gradient (ψP) to drive bulk flow through
sieve tubes. This likely involves osmoregulatory activities
at the level of the SE-CC complex (Pommerrenig et al.
2007).
In general, it would appear that phloem loading of major
osmotic species (sugars and K + ) does not constrain phloem
transport under optimal growth conditions. During periods of
abiotic stress, phloem loading can minimize the impact of
water/salt stress through osmoregulatory activities of cells
comprising the phloem-loading pathway(s) (Koroleva et al.
2002; Pommerrenig et al. 2007). Interestingly, and perhaps
surprisingly, both apoplasmic (Wardlaw and Bagnall 1981) and
symplasmic (Hoffman-Thom et al. 2001) loaders undergo maintenance
of phloem loading activities in cold-adapted plants.
This indicates that changes in the viscosity of the phloem
translocation stream may have little impact on bulk flow through
sieve tubes. In contrast, elevated temperatures can slow
translocation by callose occlusion of sieve pores (Milburn and
Kallarackal 1989). In addition, deficiencies of K + and Mg 2+ can
impact apoplasmic loading of sucrose into SE-CC complexes
(Hermans et al. 2006). In the case of K + , this is thought to reflect
a limitation in charge compensation across the SE-CC plasma
membrane which could impede the operation of the sucrose-H +
symport system (Deeken et al. 2002), whereas Mg 2+ deficiency
could lower the availability of Mg 2+ -ATP which serves as
substrate for the H + -ATPase that generates the proton motive
force to power the sucrose H + symporter (Cakmak and Kirkby
2008).
In terms of minor osmotic species, direct control of their
phloem translocation rates is determined entirely by the concentrations
to which they accumulate in SE-CC complexes.
This situation is nicely illustrated by studies performed on transgenic
peas expressing a yeast S-methylmethione transporter
under the control of the phloem-specific AtAAP1 promoter.
Here, S-methylmethione levels in developing seeds were found
to be proportional to their concentrations detected in phloem
exudates (Tan et al. 2010).
Insights into Plant Vascular Biology 325
Mechanisms of phloem unloading
The cellular pathway of phloem unloading may extend, functionally,
from SE lumens of the release phloem to sites of
nutrient utilization/storage in the particular sink organ/tissue
(Lalonde et al. 2003; Figure 13C). Within these bounds, the
cellular pathways followed circumscribe the physical conditions
under which an unloading mechanism operates. Most sink
systems investigated to date have PD interconnecting the
SE-CC complex to cells of the surrounding ground tissues,
and, thus, confer the potential for universal symplasmic unloading
(Figure 13C, I). In general, such routes for symplasmic
unloading have low densities of PD that interconnect
SE-CCs with adjacent phloem parenchyma cells. Thus, a
marked bottleneck for symplasmic nutrient delivery may exist
at this cellular interface.
Unloading routes in a variety of sink systems have
been mapped by using membrane-impermeant fluorochromes
loaded into phloem of source leaves. Upon import into the
release phloem zone, fluorochrome movement can be retained
within the vascular system of fleshy fruit during their major
phase of sugar accumulation (e.g., apple, a sorbitol transporter
(Zhang et al. 2004), grape berry, a sucrose transporter (Zhang
et al. 2006), and cucumber, an RFO transporter (Hu et al.
2011). However, more commonly, the fluorochrome moves
symplasmically out from the phloem into surrounding ground
tissues (Figure 13C, I) as found for root and shoot meristems
(Stadler et al. 2005), expanding leaves (Stadler et al. 2005),
young fruit prior to their major phase of sugar accumulation
(Zhang et al. 2006), and developing seeds in which movement
is restricted to maternal tissues (Zhang et al. 2007).
In developing fruits, during the phase of sugar accumulation,
SE-CC complexes are thought to be the site of sucrose release
into the fruit apoplasm (Zhang et al. 2004, 2006; Hu et al. 2011).
Studies conducted on tomato fruit have indicated that the
cumulative membrane surface area of SE-CC complexes would
be barely adequate to support sucrose unloading at maximal
fluxes known to be associated with membrane transport. In
contrast, using the range of reported PD-associated fluxes
(Fisher 2000), it can be shown that PD densities could readily
accommodate unloading of sucrose into surrounding phloem
parenchyma cells (Figure 13C, II). Clearly, further studies are
required to resolve whether or not phloem unloading universally
includes a symplasmic passage from SE-CC complexes to
phloem parenchyma cells in the release phloem zone, as found
for developing seeds (Zhang et al. 2007) (Figure 13C, II).
An obvious constraint on facilitated apoplasmic unloading
from SE-CC complexes is a co-requirement for a hydrolysable
transported sugar (e.g., sucrose or RFO) and an invertase
present within the cell walls of the release phloem zone. This
combination ensures maintenance of an outwardly directed diffusion
gradient for the transported sugar, due to its conversion