The Plant Vascular System: Evolution, Development and FunctionsF

324 Journal of Integrative Plant Biology Vol. 55 No. 4 2013
entry into the phloem. When operating over a prolonged period,
either of these proposed passive-loading systems would be
anticipated to cause a perturbation to metabolism within the
mesophyll cells.
Rates of phloem loading depend upon the pool size of each
transported solute available for loading, as well as the loading
and retrieval mechanisms. For sugars, sucrose (Grodzinski
et al. 1998) and polyol (Teo et al. 2006) pools are generated
in mesophyll cells, whereas RFOs are synthesized from
sucrose that enters the specialized ICs (Turgeon and Wolf
2009)(Figure 13B, II). Irrespective of sugar species and phloem
loading mechanism, during the photoperiod, transported sugars
arise from current photosynthesis and export rates are
linked positively with the sugar pool size (Grodzinski et al.
1998; Leonardos et al. 2006; Lundmark et al. 2006). During
the night, sugar pools are fed by starch reserves remobilized
from chloroplasts (Smith and Stitt 2007) and sugars released
from vacuolar storage in mesophyll cells (Eom et al. 2011)
(Figure 13B). Depending upon carbon gain by leaf storage pools
during the preceding photoperiod, remobilizing reserves during
the night can sustain sugar pool sizes and, hence, export rates
(Grimmer and Komor 1999).
In situations where source leaves are operating at suboptimal
photosynthetic activity, analyses of metabolic control
have provided estimates that source leaf metabolism exercised
approximately 80% of the control exerted over photoassimilates
transported into developing potato tubers (Sweetlove et al.
1998). However, the relationship between leaf metabolism and
export rates also depends upon prevailing source/sink ratios.
This can be illustrated by studies aimed at investigating effects
associated with CO2 enrichment. Under conditions of source
limitation, leaf photosynthetic rates are increased substantially
by CO2 enrichment, and are matched proportionately by those
of photoassimilate export (Farrar and Jones 2000). In contrast,
more attenuated responses of leaf photosynthetic rates are
elicited by CO2 enrichment under sink limitation, and these are
not proportionately matched by export (Grodzinski et al. 1998;
Grimmer and Komor 1999). The latter response suggests that,
under sink limitation, predominant control of photoassimilate
transport shifts to processes downstream of source leaf sugar
metabolism.
Estimates of membrane fluxes of sucrose loaded into SE-
CC complexes in sugar beet leaves fall into the maximal
range for plasma membrane transporter activity (Giaquinta
1983). Therefore, if sucrose transporters are indeed operating
at maximum capacity, then their overexpression might
be expected to result in enhanced rates of phloem loading
and photoassimilate export. However, overexpression of the
spinach sucrose transporter (SoSUT1) in potato, while altering
leaf metabolism, exerted no impact on biomass gain by the
tubers (Leggewie et al. 2003). This finding indicates an absence
of any constraint imposed by endogenous sucrose transporters
on phloem loading. Indeed, phloem loading can respond quite
rapidly (within minutes) to changes in sink demand (Lalonde
et al. 2003).
A striking example of the dynamic range available to the
phloem loading system is shown by studies performed on
Ricinus, a plant whose phloem sap will exude (bleed) from
severed SE-CC complexes. Here, excisions made in Ricinus
stems reduced ψP to zero in this region of the sieve tube
system. This treatment resulted in exudation of phloem sap
from the severed sieve tubes and an increase in translocation
and, hence, phloem-loading rates of sucrose, by an order of
magnitude (Smith and Milburn 1980a). This observed rapid
response is envisaged to reflect signaling from the sink region
(in this case, the site of SE-CC stem excision) to source leaves.
Here, pressure-concentration waves transmitted through interconnecting
sieve tubes (Mencuccini and Hölttä 2010) could act
to regulate transporter activity mediating phloem loading (Smith
and Milburn 1980b; Ransom-Hodgkins et al. 2003).
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sizes of RFOs are thought to prevent their backward diffusion through PD interconnecting ICs with PPCs; however, the dilated PD that
interconnect the IC-SE complexes permit forward diffusion of RFOs into the SEs (polymer trap model). (III) Passive – symplasmic loading:
Suc or Poly is proposed to move by diffusion through the symplasm, via PD, down their concentration gradients from MCs to SEs. For all
phloem-loading mechanisms, water enters (curved blue arrows) SE/CC or IC complexes through aquaporins (paired khaki ovals) (Fraysse
et al. 2005).
(C) Phloem unloading pathways from release phloem in sink organs. In all sinks, it is highly probable that imported resources are unloaded
symplasmically by bulk flow from release phloem SE-CC complexes (green-highlighted blue arrows) into adjacent PPCs. Onward resource
movement through the phloem-unloading pathway may occur by the following pathways. (I) Continuous symplasmic unloading: here,
resources (green-highlighted blue arrows) likely continue to move by diffusion through PD into surrounding phloem parenchyma (PC)
and ultimately sink cells (SC). (II) Apoplasmic step unloading: here, the phloem-unloading route involves resource transit through the sink
apoplasm due to a symplasmic discontinuity in unloading pathways at either the PPC/SC or PC/SC interface. Membrane exchange of nutrients
to, and from, the sink apoplasm occurs by transporter-mediated (khaki circles) membrane efflux and influx mechanisms, respectively. In both
cases, water exiting SE-CC complexes can enter SCs (in the case of growing sinks) or, for non-expanding storage sinks, water returns to
the xylem transpiration stream by exiting PPC/PCs (blue curved arrows) to the sink apoplasm through aquaporins (paired khaki ovals).