* Correspondence:
G.P. Zhang: zhanggp@zju.edu.cn
Running title: Advances in Cd accumulation by plants
ABSTRACT
Cadmium (Cd) contamination in the environment has become a hot issue
worldwide, as it has posed a great risk to human health via food chain.
Cd accumulation in the edible parts of crops is involved in four
processes: uptake, translocation, sequestration and redistribution,
which are all controlled by membrane transporters. In this review,
advances in the studies on the physiological and molecular mechanisms of
Cd accumulation in plants are summarized, and then the functional
evolution of Cd accumulation in plants is discussed based on oneKP
database. Plant Cd accumulation is a derived and polyphyletic trait that
has evolved convergently several times. In the course of evolution,
membrane transporter families, such as NRAMPs, HMAs, ABCCs, ZIPs, CDFs,
CAXs and OPTs, have undergone the lineage specific expansion due to gene
duplication. The orthologues of OsHMA2 and OsGLR3.4 in higher plants are
stepwisely
evolved from a common ancestor; whereas the orthologues of OsNRAMP5
evolved from a polyphyletic evolutionary lineage with several different
ancestors. In addition, abundant genetic intermixing have occurred in
the phylogenetic clusters of the orthologues of OsNRAMP5, indicating
horizontal gene transfer from one
species to another one. It may be concluded that such an evolution of Cd
accumulation in plants could provide an adaptive advantage for
colonization of plants to the novel habitats like metalliferous soil.
KEYWORDS: Cadmium, Evolution, Horizontal gene transfer, Xylem
loading, Vacuole sequestration, Transporters
1 | INTRODUCTION
Cadmium (Cd) contamination in soil has become one of the most important
environmental issues (Rai et al., 2019). It can be caused by many
artificial activities, such as application of municipal sewage sludge,
chemical fertilizers and pesticides containing Cd and mining (Clemens,
2019). It is estimated that about 30,000 tons of Cd pollutants are
discharged into the environment annually, and 13,000 tons of them are
produced from human activity (Gallego et al., 2012). Cd is easily taken
up and accumulated in plant tissues, resulting in the reduced crop yield
and harm to human health via food chain. (Ismael et al., 2019;
Rai et al., 2019).
Cd accumulation in plants may occur through
soil-plant, water-plant, and
air-plant interfaces, with soil-plant interface being the most prominent
(Shahid et al., 2017). There is a close association between soil Cd
level and plant Cd content (Khan et al. 2015). In soil-plant system, Cd
in the rhizosphere enters plant roots mainly in ionic forms, and is then
translocated to above-ground tissues, including grains
(Clemens
and Ma, 2016). As a non-essential and toxic metal element, the excessive
Cd accumulation in plants will cause various detrimental impacts on
plants, such as reducing growth, inhibiting photosynthesis and
respiration, interfering with biochemically- and physiologically-related
signaling pathways, disturbing nutrients uptake and water relations,
damaging cell membrane permeability and disrupting the cellular redox
homeostasis etc., as a consequence resulting in yield reduction and even
plant death (Shahid et al., 2017; Ismael et al., 2019). On the other
hand, excessive intake of Cd by humans through consumption of
agricultural products containing high Cd content will induce a variety
of serious diseases, including kidney cancer, breast cancer anemia,
heart failure, hypertension, cerebral infarction, proteinuria, eye
cataract formation, osteoporosis, emphysema, and renal insufficiency
(Clemens,
2019). It has been well known that crop food is the main source of Cd
exposure for human, accounting for 90% of the total dietary intake
(Khan et al., 2015). Therefore, minimizing Cd accumulation in plants, in
particular the edible parts is crucial for alleviating its harm to human
health. So a comprehensive understanding of the mechanisms underlying
the accumulation in plants is imperative for developing the crop
cultivars with less Cd accumulation.
In the last decade, a great deal of research has been done in revealing
the physiological and molecular mechanisms of Cd uptake and accumulation
(Clemens, 2019; Clemens and Ma, 2016; Manara et al., 2018). A series of
genes associated with Cd transport in plants have been identified and
functionally verified (Clemens and Ma, 2016; Shahid et al., 2017; Ismael
et al., 2019; Shi et al., 2019). Meanwhile, the specific plant genotypes
or lines with extremely low or high Cd accumulation have been developed
by genetic transformation and gene editing (Fasani et al., 2018).
Moreover, there is increasing evidences indicating that Cd accumulation
and tolerance in some plant species might have evolved under the
selection pressure for their colonization in metalliferous soils or
protecting them against herbivores or pathogens (Cappa and Pilon-Smits,
2014). However, there is no report on the relationship between
physiological/molecular mechanisms of Cd accumulation and evolutionary
adaptation. In this review, the advances in the studies on the
physiological and molecular mechanisms of Cd accumulation in plants is
summarized and the functional evolution of Cd accumulation in plants is
also discussed in terms of the most important membrane transporter
families mediating Cd accumulation.
2 | CADMIUM UPTAKE AND TRANSPORT BY
PLANTS
The mechanisms of Cd accumulation in plants have been extensively
investigated (Clemens, 2019; Clemens and Ma, 2016; Shahid et al., 2017;
Ismael et al., 2019; Shi et al., 2019). In general, Cd accumulation in
plants can be divided into 4 processes, including (1) root Cd uptake
from soil, (2) root-to-shoot translocation via xylem, (3) Cd
sequestration and (4) Cd accumulation in above-ground tissues or edible
parts through phloem.
2.1 | Cd uptake by
roots
Plants take up Cd from soil mainly by their roots, and the rate and
amount of Cd uptake in roots are dependent on Cd bio-availability or
concentration in soil (Clemens, 2006), and also controlled by genetic
factors of plants. Cd uptake by plant roots consist of two phases:
apoplastic binding and symplastic uptake (Zhao et al. 2002). In the
first phase, the positively-charged Cd2+ arises an
electrostatic interaction with the negatively-charged carboxylate groups
on cell walls, resulting in Cd accumulation in the root apoplast
(Meychik and Yermakov, 2001). It is rapid and spontaneous, suggesting no
energy requirement in this phase (a passive system). In the second
phase, Cd is symplasticly taken up in a slow active process,
which requires a great deal of
energy and is highly dependent on the metabolic activity (Sloof et al.,
1995). Cd transport across the root cell plasma membrane is the initial
step for its symplastic uptake (Yin et al., 2015). It is a
concentration-dependent process, reflected by a saturation kinetics in
the relationship of Cd uptake velocity and concentration in the medium,
indicating that Cd is taken up via a carrier
(transporter)-mediated system (Verbruggen et al., 2009). InArabidopsis and rice, for instance, many transporters from the
families of Natural Resistance-Associated Macrophage Proteins (NRAMPs,
such as OsNRAMP1, OsNRAMP5, and AtNRAMP6) and Zinc/Iron-regulated
transporter-like Protein (ZIP, such as AtIRT1) transporters are
responsible for Cd transport in root cells (Schaaf et al., 2004; Lux
et al., 2011; Sasaki et al., 2012). In addition, Cd may also enter root
cells through the transport pathway for Ca (White and Broadley, 2003; Li
et al., 2012; Chen et al., 2018), because of their similarities in
charge and ionic radius. Adding La3+ and
Gd3+ (the potent Ca channel inhibitors) or increasing
Ca concentration in the culture solution suppressed the
metabolically-dependent Cd uptake substantially in the Zn
hyperaccumulatorThlaspi
caerulescens (Zhao et al. 2002), the halophyte Suaeda salsa (Li
et al., 2012) and rice (Chen et al., 2018). Recently, one member of the
major facilitator superfamily (MFS), OsCd1, was also detected to be
associated with root Cd uptake in rice (Yan et al., 2019). However,
although a great number of membrane proteins have been demonstrated to
be involved in Cd uptake, little is known about transport of Cd across
plant root plasma membranes at the molecular level.
2.2 | Root-to-shoot Cd
translocation
After its uptake at the root epidermis or exodermis, Cd is radially
transported across the cortex, endodermis, and pericycle cells, and then
loaded into root xylem for the subsequent translocation from root to
shoot via xylem (Lu et al., 2009; Ueno et al., 2008; Uraguchi et
al., 2009b). Loading Cd into root xylem is a crucial step for Cd
translocation to the aerial plant parts (Uraguchi et al., 2009b; Ismael
et al., 2019). The radial movement of Cd toward the root xylem occursvia symplastic and/or apoplastic transport in the form of free
Cd2+ or Cd-complexes with various chelates (Shahid et
al., 2017). Symplastic transport is considered as an energy-consuming
(positive) pathway involving in both influx and efflux transporters
(Clemens and Ma, 2016). Apoplastic transport is a passive pathway,
usually driven by transpiration (Qiu et al., 2012). It was suggested
that symplastic transport play the dominant role in the radial transport
of Cd (Lu et al., 2009; Ueno et al., 2008). However, a recent study onSedum alfredii found that apoplastic pathway contributed up to
37% of Cd transported to the xylem (Tao et al., 2017). After crossing
the barriers from root epidermis to root cortex, either free
Cd2+ or Cd-chelates may enter symplasm and are then
loaded into root xylem (Gallego et al., 2012). The xylem loading of Cd
in roots is an energy-consuming process because it occurs against
membrane potential (Clemens and Ma, 2016), and is mediated by heavy
metal P1B-ATPases (HMAs) and possibly also by YSL proteins (Lux et al.,
2011; Ismael et al., 2019).
2.3 | Cd sequestration
Cd sequestration has a significant contribution to preventing Cd
translocation, thereby reducing Cd accumulation in cereal grains. The
main sites for Cd sequestration in plants are cell walls and vacuoles.
Call wall is the “first line of defense” against toxic metals from the
external environment. When captured by root cells, metal ions are
largely bound by some components of cell walls, such as cellulose,
hemicellulose, lignin, and pectin (Shi et al., 2019). As a result, the
highest Cd concentration in root tissues occurs in apoplasm,
particularly in the cell wall of rhizodermis and cortical cells (Lux et
al., 2011). Such binding of Cd to cell walls can efficiently prevent Cd
from being transported across the plasma membrane into protoplasts,
thereby reducing Cd translocation between cells and tissues.
Within the root cells, Cd is mainly located in vacuoles, which are
generally considered to be the main storage site for metals (Salt and
Rauser, 1995). Wu et al. (2005) found that 51% of Cd in barley roots
was present in the soluble fraction of vacuole, and 36% was present in
cell wall. After entering aerial plant parts, Cd is also mainly
sequestered in the vacuoles of parenchyma cells in the leaf mesophyll,
stem pith, and cortex (Qiu et al. 2011; Tian et al., 2017). Obviously Cd
sequestration into vacuoles plays a vital role in reducing Cd
concentrations in cytoplasm and alleviating Cd injury (Shi et al.,
2019). Several families of transporters have been identified to be
responsible for vacuolar sequestration of Cd, such as HMAs,
Ca2+ exchangers (CAXs), NRAMPs, MTPs and ATP-binding
cassette subfamily C proteins (ABCCs) (Korenkov et al., 2007; Park et
al., 2012; Sharma et al., 2016). It is generally assumed that
Cd2+ in cytosol firstly form the low molecular weight
(LMW) complexes by binding with metal ligands, such as glutathione
(GSH), phytochelatins (PCs), metallothioneins (MTs), nicotianamine,
organic acids and amino acids, and subsequently the complexes are
transported into vacuoles, where more Cd2+ and
thiol-containing chelators like GSH and PCs are incorporated to produce
the high molecular weight (HMW) complexes (Zhang et al., 2018). In
addition, the formation of Cd-malate complex in vacuoles is also found
to reduce the subsequent Cd efflux from vacuole to cytoplasm (Ueno et
al., 2005).
2.4 | Cd accumulation in shoots and grains
Cd accumulation in shoots and grains (the edible parts in cereals) is
the final destination of Cd transportation, which consists of three
processes, including xylem unloading, phloem translocation and
inter-vascular transfer
(Clemens
and Ma, 2016). Like xylem loading of Cd in root, Cd xylem unloading in
shoot also occurs via both apoplastic and symplastic transport
(Clemens et al., 2002). Phloem translocation represents the main pathway
of Cd accumulation in plant shoots and grains. It was reported that Cd
in phloem sap is mainly complexed with nicotianamine, glutathione (GSH),
and phytochelatins (PCs) (Mendoza‐Cózatl et al., 2008). However, how
these Cd-chelates are loaded into the phloem is poorly understood and no
responsible transporter has been identified up to date (Khan et al.,
2014).
Inter-vascular transfer is closely associated with Cd accumulation in
grains (Clemens and Ma, 2016). In cereals, nodes are the complex but
well-organized vascular systems, consisting of two major vascular
bundles: enlarged vascular bundles (EVBs) and diffuse vascular bundles
(DVBs) (Yamaji and Ma, 2014; Clemens and Ma, 2016). EVBs come from the
lower nodes and are connected to leaves, whereas DVBs surrounding the
EVBs start at the node and are connected to the upper nodes or panicles
(Clemens and Ma, 2016). Fujimaki et al. (2010) performed a noninvasive
detection of Cd in rice plant, and found that Cd was more concentrated
in the nodes than in the internodes. In rice, increasing evidences
suggest that phloem loading by inter-vascular transfer from the EVBs to
the DVBs in the node I is a major pathway for Cd movement toward grains
(Yamaji and Ma, 2014). OsHMA2 and low-affinity cation transporter 1
(OsLCT1) are involved in the inter-vascular transfer, with OsHMA2
loading Cd into the phloem of EVBs and DVBs and OsLCT1 exporting Cd from
phloem parenchyma cells into the sieve tubes (Uraguchi et al., 2011;
Yamaji et al., 2013). However, the molecular mechanisms underlying Cd
distribution in eudicots shoots is still unclear.
3 | CADMIUM
TRANSPORTERS
Since Ca is a non-essential element for plants and interferes with the
uptake of other ions, it is likely to enter plant cells through the
transporters for essential elements such as Fe2+,
Zn2+, and Mn2+, due to the
similarity of Cd2+ and these ions in chemical and
physical properties. In recent decades, a large number of genes
conferring Cd transportation across membranes in plants has been
identified and functionally verified (Clemens and Ma, 2016; Shahid et
al., 2017; Ismael et al., 2019; Shi et al., 2019). These transporters
belong to Natural Resistance-Associated Macrophage Proteins (NRAMPs),
Heavy Metal ATPases (HMAs), Zinc/Iron-regulated transporter-like
Proteins (ZRT1/IRT1-Like Protein, ZIPs), Cation Diffusion Facilitators
(CDFs), oligopeptide transporter family (OPTs), ATP-binding cassette
subfamily C proteins (ABCCs) and Cation/H+ Exchangers
(CAXs). The functions of these transporters, including uptake,
translocation, sequestration, and distribution of Cd in plants, and
their tissue-specific localization and substrate specificity are
summarized in Table 1 and Table S1.
3.1 | NRAMPs
NRAMPs represent a family of metal transporters that are located at the
membrane of root cells and evolutionarily conserved in a wide range of
organisms, including bacteria, fungi, plants, and animals (Uiiah et al.,
2018). In plants, NRAMP genes are participated in uptake of the
divalent cations, such as Fe2+,
Mn2+, Cu2+, Zn2+,
and Cd2+ as well. In Arabidopsis , six NRAMP
family members have been identified, with AtNRAMP3 andAtNRAMP4 being localized at tonoplast and responsible for
Cd2+ efflux from vacuole to the cytosol (Lanquar et
al., 2005). In rice, OsNRAMP1 and OsNRAMP5 are plasma membrane
(PM)-localized transporters involved in taking up Cd from the external
solution to root cells (Takahashi et al., 2011; Sasaki et al., 2012).
The knockdown or CRISPR/Cas9-mediated editing of OsNRAMP5 caused
a dramatic reduction of Cd and Mn concentrations in both rice roots and
shoots (Sasaki et al., 2012; Tang et al., 2017). However, OsNRAMP3,
OsNRAMP4 and OsNRAMP6 have no ability of Cd transportation (Yamaji et
al., 2013; Peris-Peris et al., 2017; Xia et al., 2010). In barley,
HvNRAMP5, which shares 84% identity with OsNRAMP5, can also mediate Cd
uptake (Wu et al., 2016). In the hyperaccmulator Noccaea
caerulescens , NcNRAMP1 is one of the main transporters involved in the
influx of
Cd2+across the endodermal PM, and thus plays a key role in
Cd2+ influx into the stele and contributes to Cd
root-to-shoot transport (Milner et al., 2014).
3.2 | HMAs
HMAs, also known as P1B –ATPase, are involved in
transporting cations across the membrane by consuming energy from ATP
hydrolysis (Williams and Mills 2005). Eight HMA members have been
identified in Arabidopsis , with AtHMA1-AtHMA4 showing the ability
of transporting divalent cations like Cd2+,
Zn2+ and Pb2+ (Williams and Mills,
2005). Of them, AtHMA2 and AtHMA4 are predominately
expressed in the tissues surrounding the vascular vessels of roots, and
they mediate Cd2+ efflux from xylem parenchyma cells
to xylem vessels, which is necessary for the root-to-shoot Cd
translocation (Mills et al. 2003). In the hyperaccumulator Thlaspi
caerulescens, Sedum plumbizincicola and Arabidopsis halleri ,HMA4 have much more gene copy numbers and transcript levels than
that in Arabidopsis thaliana (Craciun et al., 2012; Hanikenne et
al., 2008; Liu et al., 2017), and it is a candidate in determining the
evolution of Cd hyperaccumulator phenotype (Hanikenne et al., 2008). In
rice, OsHMA2 is localized at PM mainly in root cells and has been proven
to play the crucial role in Cd xylem loading and root-to-shoot
translocation, and the loss of its function significantly decreases Cd
accumulation in leaves and grains (Satoh-Nagasawa et al., 2012;
Takahashi et al., 2012). OsHMA3 is a tonoplast-localized transporter and
involved in restricting Cd translocation by mediating Cd sequestration
into the vacuoles (Miyadate er al., 2011). The lose-of-function of
OsHMA3 could cause high Cd accumulation in rice shoots and grains (Yan
et al., 2016), whereas its overexpression shows a great opportunity to
produce Cd-free rice through reducing Cd concentration in brawn rice by
94-98% (Lu et al., 2019). In addition, several recent studies suggested
that the natural variation in the promoter or coding region of HMA3
contributes to the genotypic difference in Cd accumulation in rice andBrassica rapa (Liu et al., 2019; Zhang et al., 2019).
3.3 | ZIPs
ZIPs family members are generally involved in Cd uptake and
translocation in plants (Colangelo and Guerinot, 2006). IRT1 is the
first identified member of the ZIP family in Arabidopsis , and
participates in taking up Fe2+,
Zn2+, Cu2+, Ni2+,
and Cd2+ from soil (Vert et al., 2002). In rice, 17
ZIPs transporters have been identified. OsIRT1 , which is highly
homologous to AtIRT1 , is predominantly expressed in roots and
up-regulated by Fe deficiency and Cd exposure (Bughio et al., 2002; Chen
et al., 2018). Recently, Zheng et al. 2018 showed a distinct difference
between Arabidopsis and rice in the expression profiles of ZIPs
genes in responses to Cd stress. In addition, other ZIP transporters,
like OsZIP1 and OsZIP3, have been also proved to be involved in Cd
uptake in rice (Zheng et al., 2018). It is noteworthy that the
involvement of ZIP genes in Cd uptake was also found in
hyper-accumulator plants. In Noccaea caerulescens ,NcZNT1 , a homolog of AtZIP4 , mediates low-affinity Cd
uptake when expressed in Saccharomyces cerevisiae zhy3 cells
(Pence et al. 2000). Recently, it was reported that NcZNT1 is a
PM-localized Zn2+/Cd2+ transporter
and its promoter is mainly active in cells of the cortex, endodermis,
and pericycle of roots in Noccaea caerulescens (Lin et
al., 2016).
3.4 | CDFs
CDF proteins, also known as Metal Tolerance Proteins (MTPs), are a
family of heavy metal transporters involved in the transport of
Zn2+, Cd2+, and
Co2+ (Williams et al., 2000). They have been identified
in the diverse organisms, including bacteria, fungi, animals, and
plants. The CDFs found in plant cells, generally named as MTPs (Fu
et al., 2017), are known to mediate heavy metals efflux from the
cytoplasm either to the extracellular space or to vacuoles and
organelles (Peiter et al., 2007). MTPs consists of seven phylogenetic
groups, with Zn-CDFs in groups 1 (MTP1–MTP4), 5 (MTP5) and 12 (MTP12);
the Fe/Zn-CDFs in groups 6 (MTP6) and 7 (MTP7); and Mn-CDFsg in groups 8
(MTP8) and 9 (MTP9–MTP11) (Gustin et al., 2011). In rice, OsMTP1 has
been demonstrated to be a PM-localized transporter involved in
translocation of Cd and other heavy metals in both roots and shoots
(Yuan et al., 2012). Other MTPs, such as TgMTP1 from Thlaspi
goesingense (Kim et al., 2004), CsMTP1 and CsMTP4 from Cucumis
sativus (Migocka et al., 2015), and CitMTP1 from Citrus sinensis(Fu et al., 2017), have been proved to be involved in Cd sequestration
into vacuoles or efflux from root cells.
3.5 | OPTs
OPT family, which contains Yellow Stripe-Like (YSL) transporters, is
involved in transporting metal-nicotianamine (NA) complexes through the
plant cell membrane. Thus, when Cd2+ is chelated, it
can be taken up through the OPT or YSL proteins (Zheng et al., 2018). To
enhance the availability of metal ions in rhizosphere, plant roots
secrete LMW organic acids, such as mugineic acids (Mas) and
phytosiderophore (PS), to form the metal-ligand complexes, which are
then transported by YSL transporters (Negishi et al., 2002). This
strategy is very efficient for some species of Poaceae to take up Fe
from Fe-deficient soils (Morrissey and Guerinot, 2009). In addition,
YSLs also play an important role in Cd transport. In Zea mays ,
ZmYS1 has been suggested to transport the complexes of Cd-PS and Cd-NA
at a low rate (Schaaf et al., 2004). Two orthologues of ZmYS1isolated from rice and Cd hyperaccumulator Solanum nigrum ,OsYSL2 and SnYSL3 , have beenfound to transport Cd-NA
complex when heterologously expressed in yeast (Koike et al., 2004;
Ishimaru et al., 2010; Feng et a., 2017).
3.6 | ABCCs
ABC is one of the largest protein families in organisms (Higgins, 1992)
and it has various substrates, including carbohydrates, lipids,
xenobiotics, antibiotics, drugs, and heavy metals (Martinoia et al.,
2002).
Unlike
NRAMP3/4, HMA3 and CAX2/4 transporting free Cd2+ ions,
ABCCs are found to transport the Cd-PCs complex (Zhang et al., 2018). InArabidopsis , AtABCC1 and AtABCC2 are responsible for the
transport of Cd-PCs into the vacuoles (Park et al., 2012).
Likewise,
AtABCC3 has been also suggested to mediate transport of Cd-PC complex
(Bovet et al. 2003; Brunetti et al., 2015). Besides ABCCs, some other
members of ABC transporters also confer Cd tolerance. AtABCG36/AtPDR8, a
member of the pleiotropic drug resistance (PDR) subfamily of ABC
transporters in Arabidopsis , is proposed to have a role in Cd
tolerance by pumping Cd2+ or Cd complexes out of the
plasma membrane of root epidermal cells (Kim et al., 2007). AtATM3,
which belongs to the mitochondria subfamily of Arabidopsis ABC
proteins, contributes to Cd tolerance by mediating the transport of
glutamine synthetase-conjugated Cd across the mitochondrial membrane
(Kim et al., 2006). In rice, OsABCG36/OsPDR9 has been recently
demonstrated to be involved in Cd tolerance by exporting
Cd2+ or Cd conjugates from the root cells (Fu et al.,
2019).
3.7 | CAXs
The CAXs are tonoplast-localized transporters that export cations out of
the cytosol to maintain ion homeostasis across biological membranes
(Pittman et al. 2002). Most of CAX members are calcium
(Ca2+) specific. However, two CXAs identified inArabidopsis , AtCAX1 and AtCAX2, have been found to be capable of
pumping Ca2+ and other cations like
Cd2+, Zn2+ and
Mn2+ into vacuoles (Korenkov et al., 2007; Korenkov et
al., 2009).
Wu
et al. (2011) reported that the ectopic expression of AtCAX1 inPetunia significantly increased Cd tolerance and accumulation (Wu
et al., 2011).
In
the Cd hyperaccumulator Arabidopsis halleri ,
Cd
tolerance is highly associated with the expression of AhCAX1(Baliardini et al., 2015), suggesting an involvement of AhCAX1 in
conferring Cd tolerance in this plant. A CAX2-like protein in the
hyperaccumulator Sedum alfredii , SaCAX2, confers Cd tolerance and
accumulation when heterologously expressed in yeast and tobacco (Zhang
et al. 2016).
3.8 | Other
transporters
In addition to the above transporter families, some other transporters
are also involved in Cd transport. OsLCT1, a rice homolog of wheat low
affinity cation transporter 1, is localized at PM of the cells
surrounding the EVBs and DVBs of node 1 and the phloem parenchyma cells
of DVBs (Uraguchi et al., 2011). It mediates the efflux of various
cations including Ca2+, Cd2+,
K+, Mg2+, and
Mn2+, with a high affinity for
Cd2+(Uraguchi et al., 2011). Knockdown of OsLCT1 leads to a reduction
up to 50% of grain Cd in rice plants grown in Cd contaminated soil,
indicating that OsLCT1 is involved in xylem-to-phloem distribution of Cd
(Clemens and Ma, 2016). Recently, a gene belonging to the major
facilitator superfamily, OsCd1 , was proved to be involved in root
uptake and grain accumulation of Cd in rice (Yan et al., 2019).
Furthermore, a natural variation in OsCd1 caused by a missense
mutation was found to be associated with the divergence of grain Cd
accumulation between Indica and Japonica rice . Luo
et al. (2018) identified a QTL in rice, namely CAL1, which encodes a
defensin-like protein. CAL1 is preferentially expressed in root
exodermis and xylem parenchyma cells, and acts by chelating Cd in the
cytosol and facilitating Cd secretion into apoplast, thus lowing
cytosolic Cd concentration (Luo et al., 2018).
Because
of sharing a similarity with Ca2+ in charge and ionic
radius, Cd2+ can enter the plant symplast by passive
transport through channel proteins transporting Ca2+(Perfus-Barbeoch
et al., 2002; Li et al., 2012; Chen et al., 2018). Indeed, several kinds
of calcium-permeable channels, such as depolarization-activated calcium
channels (DACCs), hyperpolarization-activated calcium channels (HACCs),
and voltage-insensitive cation channels (VICCs),
are
capable of transporting Cd2+. Increasing evidences has
been obtained using channel blockers and flux measurement to supporting
the effects of Ca on Cd uptake and accumulation in plants
(Perfus-Barbeoch et al., 2002; L.Z. Li et al., 2012; Chen et al., 2018).
However,
the functions of these channels in facilitating Cd transport is poorly
understood.
In
a recent study on rice, the expression of the genes belonging to the two
Ca channel families, annexins and glutamate receptors (GLRs), was shown
to co-segregate with Cd2+ influx and uptake by root
cells (Chen et al., 2018), suggesting the possibility to identify the
candidate channels responsible for Cd transport.
4 | EVOLUTION OF CADMIUM ACCUMULATION IN
PLANTS
4.1 | Phylogenetic variation in Cd accumulation
in plants
The great variation in Cd accumulation has been found not only among
species, but also among genotypes within a species (Cappa and
Pilon‑Smits, 2014).
Algae
constitute an important component of our environment and ecosystem as a
primary producer, contributing to nearly 40% of the global productivity
of biomass (Issa et al., 2016). Although no evidence proves Cd is
necessary for growth of algae, they have the ability to concentrate Cd
from the environment, with a manner of algae species dependent (Klimmek
et al., 2001). In fresh water green algae (Chlorophyta), such asScenedesmus
spp. (Scenedesmaceae) andSpirogyra
spp. (Zygnemataceae), the maximum concentration of Cd ranges between
3.0 to 11.4 mg/g dry biomass at 1.0-40.0 mg/L Cd in wastewater.
(Brahmbhatt et al., 2012). However, the marine brown algae (Ochrophyta),
such as Ecklonia radiate (Lessoniaceae),Macrocystis
pyrifera (Laminariaceae), Laminaria digitata (Lessoniaceae) andSargassum spp. (Sargassaceae) have been shown to be the strong
biosorbents of Cd2+, with the highest Cd concentration
ranging from 76.4 to 1634 mg/g dry biomass (Davis et al., 2004; Park and
Lee, 2002). Such a high capacity of Cd2+ adsorption
for these marine brown algae could be attributed to high alginate
content in cell wall matrix, as alginate is a biopolymer with high
affinity for divalent metals (Davis et al., 2004; Park and Lee, 2002).
On the other hand, the ability of algae to absorb Cd2+is strongly influenced by water pH. In the freshwater green algaPseudokirchneriella
subcapitata (Selenastraceae), the intracellular flux of
Cd2+ is at least 20 times higher at pH 7.0 than at pH
5.0 (Vigneault and Campbell, 2005). The similar result has been observed
inScenedesmus
obliquus (Coelastraceae), with the highest value of Cd absorption
occurring at pH7.0 (Monteiro et al, 2009). Nevertheless, for the marine
brown alga Ecklonia radiate (Lessoniaceae) considerable Cd uptake
occurs at the pH ranging 2.0-6.0 and the maximum at pH 4.0 (Park and
Lee, 2002).
Bryophytes are the first green plants to colonize the terrestrial
environment (Nickrent et al. 2000), and they are usually divided into
three large clades: the liverworts (Marchantiophyta), mosses
(Bryophyta), and hornworts (Anthocerophyta) (Shaw et al. 2011). Both
mosses and liverworts possess the ability to absorb heavy metal ions
over their entire surface, due to the lack of cuticle layer, pronounced
ion-exchange property and a large surface-to-weight ratio (reviewed by
Stanković et al., 2018). Thus, both mosses and liverworts have been
widely used as the biomoinitor or bioindicator of heavy metal pollution
in both terrestrial and aquatic environments (Mahapatra et al., 2019;
Stanković et al., 2018). Nevertheless, this ability is highly
species-specific and also strongly dependent on the environmental
conditions. Vukojević et al. (2005) reported that two moss species,Bryum capillare and Ceratodon purpureus , could accumulate
up to 0.1% Cd DW (appx.1125-1250 mg/kg) in their shoots. However, in
other two moss species Fabriona ciliaris and Leskea
angustata , Cd concentrations only varies from 0.1 to 7.3 mg/kg, with an
average value of 1.3 mg/kg (Macedo‑Miranda et al., 2016). Furthermore,
Wells and Brown (1990) found that in the moss Rhytidiadelphus
squarrosus low pH not only reduced the extracellular binding of Cd, but
also inhibited its intracellular uptake.
Ferns and
lycophytes
are the largest groups in the vascular plants beside the seed plants,
consisting of about 10,578 and 1,338 species, respectively (Pteridophyte
Phylogeny Group I, 2016). They play the important role in early land
plant evolution (Pryer et al., 2001), and are remarkably adapted to a
wide range of environments, including both tropical and cold temperate
climates, alpine and lowland regions, as well as aquatic and xeric
conditions (Mehltreter, 2008). In general, both ferns and lycophytes can
accumulate a large amount of Aluminum (Al) and Arsenic (As), but they
have much less Cd accumulation (Meharg, 2002; Schmitt et al., 2017).
However, Arora et al. (2006) measured Cd concentrations in threeAzolla (a small aquatic fern) species, and found thatAzolla would accumulate Cd as high as 2759 µg/g in shoot when
exposed to 10 mg/L Cd, suggesting a potential of Azolla in Cd
hyperaccumulation.
Gymnosperms are an ancient and
widespread plant clade, which represents four of the five main lineages
of seed plants, including cycads, ginkgos, gnetophytes, and conifers (De
La Torre et al., 2017). Gymnosperm lineages separated from each other
during the Late Carboniferous to the Late Triassic (311–212 Mya),
earlier than the occurrence of the earliest extant angiosperms (around
300 Mya) (Magallón et al., 2013). Living gymnosperms comprise only a
little more than 1000 species, with conifers (pines, cypresses and
relatives) being the largest group (Wang and Ran, 2014). The available
research on Cd accumulation in gymnosperms is mostly focused on
conifers. Kim et al. (2003) reported that Pinus sylvestris would
accumulate Cd up to 33.2 mg/kg in shoots under the treatment of 10 mg/kg
Cd for 11 weeks. In a later study, however, another Pinusspecies, Pinus pinaster, was found to accumulate only 11.9 mg/kg
Cd in shoots when exposed to 15 mg/kg Cd for 6 months (Sousa et al.,
2014). Hashemi and Farajpour (2016) found that Picea abies, grown
in the metal contaminated soils (Cd 6.8 mg/kg), could accumulate 1.5
mg/kg Cd in saplings, whereas Österås and Greger (2006) found the plant
could accumulate Cd up to 72.4 mg/kg in barks and 26.1 mg/kg in wood
after exposure to 0.5 μM Cd for 3 months. Guo et al. (2016) showed thatPlatycladus orientalis exhibited an exceptional ability of Cd
tolerance, accumulating about 69.3 mg/kg Cd in stems and 406 mg/kg in
roots after exposure to 100 mg/kg of soil for 220 days. Recently, Zeng
et al. (2018) reported that the growth of Platycladus orientaliswas significantly inhibited under the soil containing 9.6 mg/kg Cd, and
accumulated over 2 mg/kg Cd in stems and about 41.5 mg/kg in roots.
Although the results of Cd accumulation were not consistent, both
authors have suggested that Platycladus orientalis is a promising
plant for phytostabilization of Cd-contaminated soil. In addition, a
hybrid larch shows an extraordinary potential for Cd phytoextraction, as
it can tolerate a 4-week exposure to 0.25 mM Cd (or 1-week exposure to
1.5 mM Ca) and accumulate as high as 208-220 mg/kg Cd in shoots (Bonet
et al., 2016; Moudouma et al., 2013).
Angiosperms, appeared during the Early Cretaceous period (around 10-30
Myr), are the largest and most diverse group of vascular plants,
consisting of about 400-500 families and perhaps as many as 400,000
species (Taylor et al., 2009). Angiosperms represent approximately 80%
of all known living plants, including five major groups: Eudicots,
Monocots, Magnoliids, Chloranthales, and Ceratophyllales ( APG IV,
2016). Angiosperms are able to occupy any environment on the earth, such
as high mountaintops, deep oceans, freezing tundras, and warm, wet
rainforests as well (Field and Arens, 2005). It is well documented that
the angiosperm ecological incursion is highly driven by the
environmental circumstances and biotic factors (Field and Arens, 2005).
Broadley et al. (2001) summarized the early records of shoot Cd content
in
angiosperms,
founding a significant variation in shoot Cd content among the tested
108
angiosperm
species. All available results indicate that there is a large difference
in absorbing Cd from the environment among the angiosperms. In fact,
about 20 angiosperm species (~10 families) have been
already identified as Cd hyperaccumulators (Cappa and Pilon‑Smits, 2014;
Reeves et al., 2017; Qiu et al., 2012; Xu et al., 2020). These Cd
accumulators are not randomly distributed over the families of
angiosperms, and mainly belong to the families of
Brassicaceae
and Asteraceae. Two Brassicaceae species, Arabidopsis halleri andThlaspi caerulescens , which are the most intensively studied
species of Cd hyperaccumulating plants, also show an extraordinary
ecotypic variation in Cd accumulation (Reeves et al., 2018; Verbruggen
et al., 2013). Likewise, the Cd hyperaccumulator Sedum alfrediiexhibits the fixed ecotypic difference in Cd sequestration and
translocation (Cappa and Pilon‑Smits, 2014; Reeves et al., 2018),
indicating the local adaptation of these species to the natural habitats
(Reeves
et al., 2018), or probably to the anthropogenic metal pollution (Sobczyk
et al., 2017).
Overall, plants, especially angiosperms, display a wide adaptation to
the presence of Cd in the environments. Such adaptation has occurred
throughout their evolution (Broadley et al., 2001). The phylogenetic
distribution of Cd accumulation across eight to ten orders indicates
that Cd accumulation is a derived, polyphyletic trait that evolved
convergently within eight to ten angiosperm clades (Broadley et al.,
2001; Cappa and Pilon-Smits, 2014). The similar
convergent
patterns of evolution in angiosperms have also been observed for
accumulation of other metals like selenium (Se) and nickel (Ni) etc.
(Cappa and Pilon-Smits, 2014;
Reynolds et al., 2017). Hence,
here
arises a question as to which selection pressures favor the evolution of
Cd accumulation? It is well known that the emergence of Cd
hyper-accumulation trait in some plant species like Arabidopsis
halleri , Thlaspi caerulescens and Sedum alfredii was
coincident with the appearance of anthropogenic metal-polluted sites in
the mining regions (Reeves et al., 2017; Qiu et al., 2012; Xu et al.,
2020). So it is generally believed that the colonization of plants in
the anthropogenically heavy metal contaminated soils is likely to
represent a recent event in the evolutionary history of plant species
(Hanikenne and Nouet, 2011). However, a comparison study betweenArabidopsis halleri and Arabidopsis lyrata suggests that
ecological differentiation may have occurred at the onset of speciation
in this species pair (∼5 Mya,
Koch
et al., 2000) and Arabidopsis halleri has well fostered the
spread of Cd-polluted areas long before the expansion of anthropogenic
environments (Roux et al., 2011). Therefore, Cd accumulation might thus
have evolved either on the calamine outcrops before metal pollution by
mining activities, or on nonmetalliferous soils followed by a later
colonization of metalliferous soils and an increase in metal tolerance
(Hanikenne and Nouet, 2011; Reeves et al., 2018).
4.2 | Evolution of membrane transporters in
plants
Evolution
of the membrane transporters may play an important role in adapting to
metalliferous environments in plants. As described above, there are many
membrane transporters involved in Cd accumulation in plants, mainly
including NRAMPs, HMAs, ABCCs, ZIPs, CDFs, CAXs and OPTs. Thus several
intriguing evolutionary questions arise. Are these membrane transporters
conserved in all plant lineages? Is there a stepwise evolution of
membrane transporters in plants? If yes, do they occur from
monophyletic
or polyphyletic evolutionary events? The ancestors of modern land plants
colonized the terrestrial habitat about 500 to 470 Mya. Since then, the
dramatic changes have taken place for the living environments of land
plants, with a large fluctuation of water availability, illumination,
light intensity, temperature and the concentration ratio of carbon
dioxide and oxygen, as compared to the aquatic environments for
seagrasses grown in the ocean (Chen et al., 2017). As a consequence,
an
adaptive and stepwise evolution would happen persistently for the
membrane transporters in plants.
We made a comparative genomics analysis of seven Cd transporter gene
families using 41 plant species ranging from Rhodophyte to Eudicots to
reveal the difference of these gene families accompanied by species
evolution
(Figure
1; Table 2). By applying the strict selection criteria (E-value
< 10-10 and query coverage >
50%), the OPTs protein family is no longer detected in all algae
species with the exception of Klebsormidium flaccidum , which has
only one OPT homolog (Figure 1; Table 2). Hanikenne et al. (2005)
attempted to find the YS1-like proteins in the genome sequences of green
alga Chlamydomonas reinhardtii and red alga Cyanidioschizon
merolae , but failed to identify any homolog. Likewise, a previous
phylogenetic analysis of 325 OPTs family members from prokaryotes and
eukaryotes revealed that OPT family members in eukaryotes were found
only in fungi and land plants (Gomolplitinant and Saier Jr., 2011). Thus
it may be suggested that the OPTs family have evolved after the
emergence of land plants. By contrast,
the
families of NRAMPs, HMAs, ABCCs,
ZIPs,
CAXs and CDFs are identified across all the plant species, although CAX
(in Cyanidioschyzon merolae and Mesotaenium
endlicherianum ) and ZIP (in Porphyra yezoenesis and Volvox
carteri ) homologs were not detected in several algae species (Table 2).
As the ancient gene families that
pre-date the origin of eukaryotes (Emery et al., 2012; Gustin et al.,
2011; Hanikenne and Baurain, 2014; Hanikenne et al., 2005; Montanini, et
al., 2007; Williams and Mills, 2005; Ullah et al., 2018), these Cd
transporter families seem to be conserved throughout the evolutionary
lineage of entire plantae, indicating an evolutionarily conserved
function of them in metal homeostasis. Furthermore, it is notable that
the vascular plants, including lycophytes, ferns, gymnosperms and
angiosperms, contain much more family members of NRAMPs, HMAs, ABCCs,
ZIPs, CAXs, CDFs and OPTs in their genomes than do algae and bryophytes
(liverworts and mosses) (Table 2), suggesting that these transporter
families underwent lineage specific expansion, which might be
contributed by gene duplication resulting from segmental duplication
[whole genome duplication (WGD) or duplications of large chromosomal
regions] and/or tandem duplication (Cannon et al., 2004; Liu et al.,
2012; Ullah et al., 2018). During the course of evolution, the expansion
of membrane transporter families in the vascular plants may provide an
adaptive advantage for colonizing new habitats
like metalliferous soil before
significant vascular development occurred in early land plants.
OsNRAMP5 and OsHMA2, which mediate Cd uptake and xylem loading
respectively, are recognized as the most important transporters for Cd
accumulation in rice (Clemens and Ma, 2016). In order to understand the
origin of these two Cd transporters, a phylogenetic analysis was
performed across the entire plant kingdom using oneKP database (One
Thousand Plant Transcriptomes Initiative, 2019). In the phylogenetic
tree with 396 species, the orthologues of OsHMA2 from
algae, mosses, ferns, lycophytes,
gymnosperms and angiosperms form a distinct cluster, but they are all
basal to Rhodophyta species Rhodochaete parvula(Figure 2A), indicating that this
transporter has experienced an early evolution in plants. While the
angiosperms cluster can be grouped into two sub-clusters of monocots and
eudicots, and all of them are basal toAmborella
trichopoda , which is the only living species on the sister lineage to
all other flowering plants (Amborella Genome Project, 2013). In
addition, eudicots show a closer orthologous relationship withMyristica fragrans (Figure 2A). These results indicate that
monocots and eudicots share a common origination of HMA2 transporter
from Amborella trichopoda , which can be dated back to about 130
Mya. However, they have evolved separately thereafter, forming a
monophyletic evolutionary lineage.
In phylogenetic analysis the orthologues of OsNRAMP5 proteins from 592
species are grouped into two clusters (Figure 2B). Cluster 1 includes
green algae, Glaucomphyta, Rhodophyta and mosses; and Cluster 2 contains
green algae, hornworts, liverworts, lycophytes, ferns, gymnosperms and
angiosperms. Each cluster can be further divided into three
sub-clusters; the sub-clusters in cluster 2 are deeply-branching, while
those in cluster 1 are not. In the three sub-clusters of cluster 2,
green algae form a distinct sub-subcluster; lycophytes, ferns and
gymnosperms are included in the other two sub-subclusters; whereas
hornworts, liverworts, and angiosperms can only be found in the last
sub-subcluster. In addition, the higher plants are clearly divided into
two groups, monocots and eudicots, occupying their specific ancestral
gymnosperms and basal angiosperms (Figure 2B). It may be suggested that
the orthologues of OsNRAMP5 in
higher plants underwent a polyphyletic evolutionary lineage originated
from different ancestors. Furthermore, the divergent presence of green
algae, lycophytes, ferns and gymnosperms in the phylogenetic tree
indicates a rampant occurrence of
horizontal
gene transfer during the evolution of the orthologues of OsNRAMP5
(Figure 2B), which has been previously evidenced in the studies on the
evolution of NRAMPs in bacteria (Richer et al., 2003) and OPTs in plants
(Gomolplitinant and Saier Jr., 2011). However, further studies are
necessary to make insight into the molecular mechanisms and adaptive
roles of horizontal gene transfer events in the evolution of Cd
transporters in plants.
Our previous study revealed that the expression of OsGLR3.4 was
co-segregated with Cd2+ influx and uptake into rice
roots (Chen et al., 2018). Recently, the contribution of GLR channels to
Cd2+ influx was verified using mammalian glutamate
receptor antagonists AP-5, and our results showed that net
Cd2+ influx in rice root epidermis was significantly
inhibited by AP-5 (Figure 3A). Moreover, relative expression ofOsGLR3.4 was up-regulated when rice plants were exposed to 5 and
50 μM Cd stress (Figure 3B). All these results support the assumption
that GLR channel is involved in mediating Cd uptake in rice roots (Lux
et al., 2011; Clemens, 2019). Here we present the origin of OsGLR3.4
across the entire plant kingdom (Figure 3C). Accordingly, the
phylogenetic analysis of OsGLR3.4 was conducted using 850 species-based
oneKP database. In the phylogenetic tree, the orthologues of OsGLR3.4
from Streptophyta to Eudicots formed 5 distinct clusters. Interestingly,
each phylogenetic cluster includes very specific clades of species
(Figure 3C). Among the major clusters, GLR3.4 can be traced to
Streptophyta species, and the significant presence are observed in
hormworts, liverworts, mosses, lycophytes, ferns, gymnosperms and
angiosperms (Figure 3C), in accordance with the phylogenetic analysis of
OsHMAs (Figure 2A), indicating an ancient origin of OsGLR3.4 orthologues
in plants (Bortoli et al., 2016). Moreover, angiosperms are grouped into
2 sub-clusters, with each sub-cluster containing the specific basal
angiosperms, monocots and Eudicots, suggesting that GLR3.4 could have
recently diverged into two evolutionary branches, possibly giving rise
to the distinct functions between them, adapting to Cd-contaminated
environments.
5 | CONCLUSIONS AND
PERSPECTIVES
Cd is one of the most hazardous toxic heavy metals in the environments,
posing great risks to human health. Cd accumulation in plants is
controlled by both genetic and environmental factors via affecting the
whole process, including uptake from soil, root-to-shoot translocation,
sequestration and (re)distribution in shoots. In essence, all these
processes are governed by membrane metal transporters, including NRAMPs,
HMAs, ZIPs, CDFs, OPTs, ABCCs, CAXs and some other transporters or
channels like OsLCT1, OsCd1 and CAL1. Across the entire plantae kingdom,
Cd accumulation displays a wide phylogenetic variation among species and
genotypes within a species. By applying oneKP database, the functional
evolution of Cd accumulation in plants was carefully examined,
indicating that Cd accumulation in plants is a derived and polyphyletic
trait that has evolved convergently by several times. During the course
of evolution, the membrane transporter families, such as NRAMPs, HMAs,
ABCCs, ZIPs, CDFs and CAXs, are conserved throughout the evolutionary
lineage of entire plantae species, indicating that their functions are
evolutionarily conserved for metal homeostasis. However, the OPTs
protein family is missed in algae species, suggesting that the OPTs
family may evolve after the emergence of land plants. Moreover, the
vascular plants contain much more family members of the above
transporters in their genomes than do algae and bryophytes, suggesting
that these transporter families underwent lineage specific expansion,
which might be conferred by gene duplication due to segmental
duplication and/or tandem duplication. Furthermore, the orthologues of
OsHMA2 and OsGLR3.4 in higher plants are stepwisely evolved from
monophyletic evolutionary lineage with one common ancestor; whereas the
orthologues of OsNRAMP5 came from a polyphyletic evolutionary lineage
with the different ancestors. In addition, the rampant intermixing have
occurred for the orthologues of OsNRAMP5 in the phylogenetic clusters,
indicating the horizontal gene transfer in its evolution. All these
evolutionary patterns may provide an adaptive advantage for colonization
of plants to new habitat like metalliferous soil.
Due
to lack of information on the known Cd hyperaccumulators in oneKP
database, we still have no clear answer as to whether and what extent
such evolutionary patterns of membrane transporters contributes to Cd
(hyper)accumulation in plants. Ideally, the non-accumulator, accumulator
and hyperaccumulator plants should be comprehensively compared, in terms
of genome sequencing, ecological distribution patterns and the ability
of Cd uptake and transport, so as to fully elucidate the evolutionary
mechanisms associated with the accumulation and adaptive response of Cd
in plants.
ACKNOWLEDGEMENTS
This work was supported by the National Key Technology R&D Program
(2018YFD0800200), and Jiangsu Collaborative Innovation Center for Modern
Crop Production (JCIC-MCP).
CONFLICT OF INTEREST
STATEMENT
The authors declare that they have no conflict of interest.
AUTHOR CONTRIBUTIONS
F. R. Z. and G. P. Z. planned and designed the outline of this review.
G. C. and X. H. C. prepared the figures and tables.
F. R. Z., Q. L., X. J. W. and G. P. Z. wrote the manuscript.
SUPPLEMENTARY MATERIALS
Table S1 Information of NRAMPs, HAMs, ABCCs, ZIPs, CDFs, CAXs
and OPTs families for evolutionary bioinformatics analysis.
Supplemental file 1 List of references for Table 1.
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FIGURE LEGENDS
Figure 1 Similarity heat map of key membrane Cd transporters in
different species. Genesis software was used to estimate the similarity
among protein sequences based on Tables 1 and S1. Candidate protein
sequences were selected by BLASTP searches which satisfied E value
<10-10 and query coverage
>50%. Colored squares indicate protein sequence similarity
from zero (blue) to 100% (red). White squares indicate that no
homologous genes were found.
Figure 2 Phylogenetic analysis of OsHMA2 (A) and OsNRAMP5 (B).
The mRNA sequences of OsHMA2 and OsNRAMP5 were queried from the One
Thousand Plant Transcriptome (1KP) database (https://sites.google.com/a/
ualberta.ca/onekp/). Amino acid sequence of Oryza Sativa OsHMA2
and OsNRAMP5 were employed as the query sequences to access the
transcriptome data with the criterion of E-value <
10-10 and coverage > 50% using BLASTP.
The sequences were aligned with MAFFT and the phylogenies constructed
with the online toolkit RAxML (Stamatakis, A., 2014) of CIPRES (Miller,
M.A. et al., 2010). Genes sampled from Chromia algae were used as the
outgroup (in the shade of light grayish magenta) and the root of the
tree, and the Interactive Tree of Life resource
(http://www.itol.embl.de) was used to annotate gene trees. Bootstraps
(1-100) were displayed as the width of branches (1-10 px).
Figure 3 Kinetics of Cd2+ fluxes in response to glutamate
receptor antagonists AP-5 (A), gene expression of OsGLR3.4 in response
to external Cd (B) and phylogenetic analysis of OsGLR3.4 (C). Transient
Cd2+ fluxes were measured from mature zone in rice
root in response to 50 μM Cd pretreated with or without 100 μM AP-5,
Data ±SE(n=8). Gene expression of OsGLR3.4 was quantified by
qRT-PCR under 5 or 50 μM Cd at the exposure time indicated in the
figure, , Data ±SE(n=3). Phylogenetic analysis of OsGLR3.4 was conducted
similarly as described in Figure 2.
Table 1 The identified transporters mediating Cd uptake,
translocation, sequestration and distribution in plants sequestration
and distribution in plants