[50], and failure to cross biological membranes. It is proposed that ionized groups or low lipophilicity pre-
vents entry into the SE-CC complex [51,52]. It is important to note that not all herbicides need be mobile
but can be herbicidal simply if they disrupt transport of photoassimilates from source to sink tissues.
Chlorsulfuron is one such herbicide that has been shown to disrupt transport of photoassimilates, but the
mode of its action is still unknown [53].
- Protein and Viral Movement in the Phloem
Researchers have investigated the cell-to-cell trafficking of macromolecules from the companion cells
into the sieve tube via plasmodesmata [54]. It has long been known that cell-to-cell movement of small
molecules can occur via the symplasm, but more recently it has been demonstrated that large macro-
molecules (viral-encoded movement proteins [55,56], messenger RNA [57] and plant macromolecules
[58]) can apparently enter the phloem via plasmodesmata.
Viral coat proteins are believed to interact with endogenous plasmodesmal proteins to increase the
size exclusion limit (SEL) and allow movement of virus particles from infected to uninfected neighbor-
ing cells. It appears that these proteins found in the phloem are exclusively synthesized in the companion
cells [59]. Phloem sap proteins of Cucurbita maximahave the ability to induce an increase in the SEL of
plasmodesmata by greater than 20 kDa [54]. It is hypothesized that macromolecules greater than 20 kDa
may partially unfold to facilitate transport through the plasmodesmata. The ability to transport large pro-
teins or nucleic acids via the phloem translocation pathway may help explain how many pathogenic and
developmental processes are controlled.
IV. PHLOEM LOADING
As indicated by structural differences, there appear to be two pathways by which assimilates can be trans-
ferred from the photosynthetic cells to the minor vein SE-CC complexes in the source leaf. In species pos-
sessing the type 1 minor vein configuration, this transport can occur by a symplastic route through the nu-
merous plasmodesmata that interconnect the photosynthetic cells and the phloem transport system. In
plants with type 2 configurations, which lack a high degree of symplastic interconnection, transport can
occur by a transmembrane route via the apoplast.
A. Apoplastic Phloem Loading
The textbook model of phloem loading in source leaves consists of a sequence of events starting with cell-
to-cell transport of assimilates, primarily sucrose, through mesophyll cell plasmodesmata to a site close
to the SE-CC complex. At this point, sucrose is unloaded into the apoplast, where it is actively accumu-
lated into the SE-CC complex by a proton-sucrose symport mechanism (Figure 6A). The apoplastic pro-
ton symport model of phloem loading [17,18] affords a very satisfactory mechanism for establishing the
high concentration gradient required within the phloem to drive phloem transport by Munch pressure
flow.
One of the key demonstrations of the apoplastic loading pathway is the inhibition of sucrose-proton
cotransport by inhibitors such as p-chloromercuriphenylsulfonic acid (PCMBS). In isolated leaf plasma
membrane systems [60,61] and leaf tissues [62], this compound has been shown to bind to the sucrose
carrier [63] and to prevent transfer of sucrose. In many plants, this compound will also inhibit the deliv-
ery of photosynthetically produced sucrose from the photosynthetic cells to the minor veins of leaf tissues
[62]. This finding lends significant support to the apoplastic loading theory.
Interestingly, though, only species possessing the type 2 minor vein configurations show this sensi-
tivity to PCMBS [29,64]. In these species, which include most of the important agronomic crops, sucrose
is the only sugar transported in the phloem. Therefore, apoplastic phloem loading probably best explains
delivery of sucrose to the phloem in most agronomic species. However, although there is appreciable ex-
perimental evidence in support of the apoplastic pathway, it is now becoming apparent that this model
may not hold for all crop plants.
B. Symplastic Phloem Loading
In plants with the type 1 minor vein configuration, where a symplastic route through plasmodesmata is
available for the delivery of endogenously produced photoassimilates to the minor veins, phloem loading
458 MIRANDA ET AL.