The Plant Vascular System: Evolution, Development and FunctionsF

354 Journal of Integrative Plant Biology Vol. 55 No. 4 2013
acid complexes (mugineic acids are synthesized from NA),
especially as the neutral-to-basic pH of the phloem sap is
suitable for metal-NA formation (Pich et al. 1994; von Wirén
et al. 1999; Takahashi et al. 2003). Accordingly, Zn(II)-NA and
Fe(III)-2 ′ -deoxymugineic acid complexes have been detected
in phloem sap from rice (Nishiyama et al. 2012). Furthermore,
mutants defective in NA production display lower Mn, Zn,
Fe and Cu concentrations in reproductive organs (Takahashi
et al. 2003; Curie et al. 2009). However, it is still unclear
whether this impediment to metal delivery into sink organs
is due to alterations in phloem loading and transport, per se,
or to changes in the intracellular concentrations of metals in
source tissues where NA also plays an important role in metal
chelation.
The phloem may also transport other forms of Fe; e.g., an
iron transport protein (ITP) is present in the phloem sap of
Ricinus communis (Krüger et al. 2002), but it has not yet been
found in other species. A copper chaperone protein (CCH) has
also been proposed to play a role in phloem transport of Cu
from senescing to young leaves (Mira et al. 2001). In addition,
metallothioneins (types 1, 2 and 3), proteins predominantly
regulated by Cu, also appear to function in Cu accumulation
and phloem transport during senescence (Guo et al. 2003,
2008). These proteins are also associated with Cu tolerance
(Murphy and Taiz 1997; van Hoof et al. 2001; Jack et al. 2007).
Currently, little information is available concerning the chemical
forms of Ni and Mn in the phloem sap. In R. communis, Mn
has been detected in association with low molecular weight
peptides (van Goor and Wiersma 1976), whereas Ni can be
complexed with negatively charged organic compounds with
a molecular weight in the range of 1,000–5,000 Da (Wiersma
and van Goor 1979).
The mobility of molybdenum (Mo) in the phloem varies
depending on its concentration and on plant age. Interestingly,
in wheat, Mo has been associated with the existence of “Mobinding
sites” in the phloem that, until saturated, appear to
prevent its long-distance translocation (Yu et al. 2002). B mobility
in the phloem is highly dependent on the plant species. In
plants that transport sugar alcohols, B appears to be complexed
with diols and polyols (Brown and Hu 1996; Hu et al. 1997;
Takano et al. 2008). Complexes of sorbitol-B-sorbitol, fructose-
B-fructose, sorbitol-B-fructose and mannitol-B-mannitol have
been identified in peach and celery phloem sap (Hu et al. 1997).
Enhancement of sorbitol production results in an increase of B
translocation from mature leaves to sink tissues as well as
tolerance to B deficiency. In plant species that do not produce
significant amounts of sugar alcohols, B is thought to be phloem
immobile, or only slightly mobile, and its distribution in shoots
seems primarily to follow the xylem transpiration stream (Oertli
1993; Bolaños et al. 2004; Lehto et al. 2004; Takano et al.
2008).
Vascular loading and unloading of cationic
micronutrients
Yellow Stripe-Like (YSL) proteins play important roles in the
short- and long-distance transport of microelements and their
delivery to sink tissues (Curie et al. 2009). Members of the YSL
family, AtYSL1, AtYSL2, AtYSL3, OsYSL2 and OsYSL18, are
expressed in vascular tissues (Table 3) and may have a role
in the lateral movement of Fe within the veins and in phloem
transport (DiDonato et al. 2004; Koike et al. 2004; Le Jean et al.
2005; Schaaf et al. 2005; Aoyama et al. 2009). The rice OsYSL2
can transport Fe(II)-NA and Mn(II)-NA to an equal extent (Koike
et al. 2004). OsYSL18 transports Fe(III)-deoxymugineic acid
(Aoyama et al. 2009), whereas there are contradictory reports
concerning the ability of AtYSL2 to transport Fe(II)-NA and
Cu(II)-NA (DiDonato et al. 2004; Schaaf et al. 2005). AtYSL1
seems to play a role in Fe(II)-NA translocation to seeds (Le
Jean et al. 2005). A study on the Arabidopsis double mutant
ysl1ysl3 reported reduced accumulation of Fe, Cu and Zn in
seeds, consistent with involvement of the YSL1 and YSL3
transporters in remobilization from leaves (Waters et al. 2006).
There is also evidence for a role of YSLs in the Zn and
Ni hyperaccumulation of Thlaspi caerulescens, especially for
TcYSL3 and TcYSL7, which are highly expressed around
vascular tissues particularly in shoots when compared with
their A. thaliana orthologs (Gendre et al. 2007). TcYSL3 is an
Fe(II)-NA and Ni(II)-NA influx transporter that is suggested to
facilitate the movement of these metal-NA complexes from the
xylem into leaf cells.
A number of other transporters involved in vascular loading
and unloading of microelements have also been identified
(Figure 26, Table 3). The Arabidopsis OPT3 transporter
(OligoPeptide Transporter) appears to be essential for embryo
development (Stacey et al. 2008). This protein transports Mn,
and its expression in the vascular tissue suggests a role
in Mn long-distance transport. Although yeast studies have
suggested that it can also transport Cu, OPT3 does not appear
to play a role in Zn or Cu loading, as seeds of opt3-2 plants
actually accumulate increased levels of these two metals
(Stacey et al. 2008). The opt3-2 mutant also has reduced
Fe concentrations in its seeds as well as impaired seedling
growth under Fe-deficient conditions, thus suggesting a role in
Fe loading into the seed (and perhaps even phloem-mediated
redistribution).
Another Fe efflux transporter, IREG1/FPN1 (Iron Regulated1/Ferroportin1),
is considered to function in Fe loading
into the xylem within the roots (Morrissey et al. 2009). Loss
of FPN1 function results in chlorosis, and FPN1-GUS plants
show staining at the plasma membrane of the root vascular
system. However, yeast complementation studies using FPN1
have failed, and information on the chemical form of Fe