* Correspondence:
G.P. Zhang: zhanggp@zju.edu.cn
Running title: Advances in Cd accumulation by plants
ABSTRACT
Cadmium (Cd) contamination in the environment has becoming a hot issue
in the world, as it has posed a great risk to human health through the
food chain. Cd accumulation in the edible parts of plant crops are
involved in four processes: uptake, translocation, sequestration and
(re)distribution, which are all controlled by membrane transporters. In
this review, the advance in studies on physiological and molecular
mechanisms of Cd accumulation in plants was summarized, and then the
functional evolution of Cd accumulation in plants was discussed based on
oneKP database. Plant Cd accumulation is a derived and polyphyletic
trait that has evolved convergently by several times. In the course of
evolution, the 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 in higher
plants are
stepwisely
evolved from monophyletic evolutionary lineage with one common ancestor;
whereas the orthologues of OsNRAMP5 from a polyphyletic evolutionary
lineage with several different ancestors. In addition, phylogenetic
clusters of the orthologues of OsNRAMP5 have occurred rampant
intermixing, suggestive of horizontal gene transfer. It may be concluded
that such an evolution of Cd accumulation in plants could provide an
adaptive advantage for colonization of plants to the new habitats like
metalliferous soil.
KEYWORDS: Cadmium, Monophyletic evolution, Polyphyletic
evolution, Tissue accumulation, Transporters, Vacuole sequestration
1 | INTRODUCTION
Cadmium (Cd) contamination in soil has become one of the environmental
issues receiving more and more attention in the world (Rai et al.,
2019). Cd contamination can be caused by several human activities, such
as the application of municipal sewage sludge, atmospheric deposition of
Cd, mining, application of chemical fertilizers and pesticides
containing Cd (Clemens, 2019). It is estimated that about 30,000 tons of
cadmium 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 reduced crop yield and also threatening 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 dominant (Shahid
et al., 2017). It is well documented that there is a close association
between Cd level in soil and food crops (Khan et al. 2015). In
soil-plant systems, Cd in rhizosphere enters are plant roots in ionic
forms, and then translocated into above-ground tissues, including grains
of cereal crops
(Clemens
and Ma, 2016). As a non-essential and toxic metal element, the excessive
Cd accumulation in plants will causes various detrimental impacts on
plants, such as reducing plant growth and development, inhibiting
photosynthesis and respiration, interfering with biochemical 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). In turn, by consumption of the Cd-contaminated foods, Cd intake
and accumulation occur inevitably in human body, thus arising serious
health risks, such as kidney cancer, breast canceranemia, heart failure,
hypertension, cerebral infarction, proteinuria, eye cataract formation,
osteoporosis, emphysema, and renal insufficiency
(Clemens,
2019). It has been well known that crop foods are the main sources of Cd
exposure in population, which account for 90% of the total dietary
intake (Khan et al., 2015). Therefore, controlling Cd accumulation in
plants, in particular the edible parts is crucial for reducing its
threat to human health. Accordingly, a much better understanding of the
mechanisms underlying Cd uptake, translocation, detoxification, and
accumulation is imperative.
In the last decades, the rapid advance has been made in revealing the
physiological and molecular mechanisms of Cd uptake and accumulation
(reviewed by 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 (reviewed by 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 manipulation, such as
transformation, gene editing and molecular breeding (reviewed by Fasani
et al., 2018). However, there is no review available which
systematically reports the role of heavy metal transporters in Cd
absorption and accumulation, and their evolution. In this review, the
advance in studies on the physiological and molecular mechanisms of Cd
accumulation in plants is first summarized and the functional evolution
of Cd accumulation in plants was further discussed in terms of the most
important membrane transporter families mediating Cd accumulation.
2 | CADMIUM UPTAKE AND TRANSPORT BY
PLANTS
The mechanisms for Cd accumulation in plants have been extensively
investigated, (reviewed by Clemens, 2019; Clemens and Ma, 2016; Shahid
et al., 2017; Ismael et al., 2019; Shi et al., 2019). In general, the
whole process of Cd accumulation from the growth medium (soil) to
above-ground plant parts can be divided into 4 steps, 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 can take up Cd from soil by their roots, and the rate and amount
of Cd absorption in roots are dependent on Cd bio-availability or
concentration in soil (Clemens, 2006). Meanwhile root Cd uptake is
controlled by genetic factors of plants and greatly affected by
environmental conditions. The uptake of Cd2+ 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
Cd2+accumulation of in the root apoplast (Meychik and
Yermakov, 2001). It is rapid and spontaneous, suggesting the phase of
apoplastic binding require no energy (passive system). Compared to
apoplastic binding, the second phase, symplastic uptake is a slow active
process, requiring a huge of energy
and depending 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, exhibiting the saturable kinetics in
the relationship of Cd concentration in the medium and uptake velocity,
indicating that Cd is taken up via a carrier-mediated system (Verbruggen
et al., 2009). Since it is a non-essential element for plants and
interferes with the uptake of other ions, it may be assumed that
Cd2+ is likely to enter root cells through the
transporters for essential elements such as Fe2+,
Zn2+, and Mn2+, due to the
similarity of Cd2+ to these ions in chemical and
physical properties. In Arabidopsis 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 have been demonstrated to transport Cd2+in root cells (Schaaf et al., 2004; Lux et al., 2011; Sasaki et al.,
2012). In addition, Cd2+ may also enter root cells
through the transport pathway for Ca2+ (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+ (potent Ca channel inhibitors) or increasing
the concentration of Ca (ca. 5mM) appeared to suppress 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 the uptake of Cd in plants, little is still known about
transport of Cd2+ across root plasma membranes at
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 roots to
shoots 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 occurs
via the symplastic and/or apoplastic transport of free
Cd2+ or Cd-complexes with various chelates (Shahid et
al., 2017). Symplastic transport is considered as an energy-consuming
(positive) pathway involving both influx and efflux transporters
(Clemens and Ma, 2016). Apoplastic transport is known to be a passive
pathway, usually driven by transpiration (Qiu et al., 2012). It was
suggested that the symplastic transport play the dominant role in the
radial transport of Cd to root xylem in plants (Lu et al., 2009; Ueno et
al., 2008). However, a recent study on Sedum alfredii found that
the apoplastic transport contributed up to 37% of the transported Cd
when exposed to high Cd level (Tao et al., 2017). After crossing the
barriers from root epidermis to root cortex, either free Cd ions or
Cd-chelates may enter symplasm and are then loaded into root xylem
(Gallego et al., 2012). The xylem loading of Cd in roots a
energy-consuming process because it occurs against membrane potential
(Clemens and Ma, 2016), and is mediated by heavy metal P1B-ATPases
(HMAs), such as orthologues of AtHMA2 and AtHMA4, 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 controlling Cd accumulation in the plant tissues.
The main sites for Cd sequestration in plant cells 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 banded by the functional components of cell walls, such as
cellulose, hemicellulose, lignin, and pectin (Shi et al., 2019). Many
studies found that there was the highest Cd concentration in the
apoplasm of roots, particularly in the cell walls of the rhizodermis and
cortical cells, while root cells had much lower Cd concentrations (Lux
et al., 2011). Such binding of Cd to cell walls can efficiently prevent
Cd from being transported across the plasma membrane into the
protoplasts, thereby reducing the translocation of Cd in plant cells and
tissues. Once inside the root cells, Cd is mainly concentrated in
vacuole, which is generally considered to be the main storage site for
metals in plant cells (Salt and Rauser, 1995). Some studies on the cell
fractionation have shown that Cd-sensitive plants have even higher Cd
concentrations in vacuole than in cell wall (Uraguchi et al., 2009a). Wu
et al. (2005) found that 51% of the Cd in barley root is present in the
soluble fraction of vacuole, and only 36% is present in cell wall.
After its translocation from roots to the aerial plant parts, Cd is
mainly sequestered in vacuoles of parenchyma cells in the leaf
mesophyll, stem pith, and cortex in plant shoots (Qiu et al. 2011; Tian
et al., 2017). Obviously Cd sequestration into vacuoles plays a vital
role in reducing Cd concentrations in the cytoplasm and alleviating Cd
toxicity to enzymes involved in cytosolic biochemical reactions (Shi et
al., 2019). Several families of transporters have been identified to be
responsible for the process of vacuole sequestration, 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 Cd ions in
the cytosol first 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 are transported into the vacuole, 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
the 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
Following the process of root uptake and root-to-shoot translocation,
the accumulation of Cd in shoots and grains (the edible part in cereals)
is the final destination of Cd, which consists of three processes,
including xylem unloading, phloem translocation and inter-vascular
transfer
(Clemens
and Ma, 2016). Corresponding to the 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 the 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 up to date, and none responsible
transporter has been identified (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 suggests that phloem loading
by inter-vascular transfer from the EVBs to the DVBs in 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 dicots shoots is
still unclear.
3 | CADMIUM
TRANSPORTERS
As a non-essential element, Cd normally enters into plant roots through
the same pathways as essential or beneficial elements, such as
Zn2+, Fe2+ and
Mn2+ (Clemens, 2006). In recent decades, a large
number of genes conferring Cd transportation across membrane in plants
have 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). All these transporters
are involved in uptake, translocation, sequestration, and distribution
of Cd in plants, and their tissue-specific localization and substrate
specificity are summarized in Table 1.
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, animals, and plants (Uiiah et al.,
2018). In plants, NRAMP genes are participated in the 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 and AtNRAMP4 being localized
at tonoplast and responsible for Cd2+ efflux from the
vacuole to the cytosol (Lanquar et al., 2005). In rice, OsNRAMP1 and
OsNRAMP5 are plasma membrane (PM)-localized transporters and
participated 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
appeared having 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 the uptake of Cd
(Wu et al., 2016). In the hyperaccmulator Noccaea caerulescens ,
NcNRAMP1 is one of the main transporters involved in the influx of Cd
across the endodermal PM, and thus plays a key role in Cd 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, have a great
contribution to transporting cations across the membrane by consuming
energy from ATP hydrolysis (Williams and Mills 2005). There are eight
HMA members identified in Arabidopsis, with AtHMA1-AtHMA4 showing the
ability of transporting divalent cations like Cd2+,
Zn2+ and Pb2+ (Williams and Mills,
2005). Among them, AtHMA2 and AtHMA4 are predominately expressed in the
tissues surrounding the vascular vessels of roots and other tissues such
as stems and leaves, and they mediate efflux of Cd from xylem parenchyma
cells to xylem vessels and are necessary for the root-to-shoot Cd
translocation (Mills et al. 2003). In the hyperaccumulator T.
caerulescens, S. plumbizincicola and A. halleri , HMA4 shows much higher
gene copy numbers and transcript levels than that in A. thaliana(Craciun et al., 2012; Hanikenne et al., 2008; Liu et al., 2017), and is
considered to be a candidate in determining the evolution of Cd
hyperaccumulator phenotype (Hanikenne et al., 2008). In rice, OsHMA2 is
localized to 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 by
reducing Cd concentration in brawn rice by 94-98% (Lu et al., 2019). In
addition, some 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 and Brassica 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
participated 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). A recent comparative study of the genome-wide expression
profiles revealed a distinct difference between Arabidopsis and rice in
the expression profile of ZIPs genes in response to Cd stress (Zheng et
al., 2018). 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
in hyperaccumulators has also been suggested. In N. caerulescens ,
NcZNT1, a homolog of AtZIP4, mediates low-affinity Cd uptake when
expressed in Saccharomyces cerevisiae zhy3 cells (Pence et al.
2000). Recently, it has been demonstrated 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 N. 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+, and has been identified in the diverse organisms,
including bacteria, fungi, animals, and plants. (Williams et al., 2000).
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 into the 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 also been proved to be involved in Cd
sequestration into vacuoles or Cd 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 Cd is chelated, it can be taken up
through 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
Gramineae plants 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 ZmYS1 isolated from rice and Cd hyperaccumulatorSolanum nigrum , OsYSL2 and SnYSL3, have been also reported to
transport NA-complexes containing Cd 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 living organisms (Higgins,
1992), which have various substrates, including carbohydrates, lipids,
xenobiotics, antibiotics, drugs, and heavy metals (Martinoia et al.,
2002).
Unlike
NRAMP3/4, HMA3 and CAX2/4 transporting the free Cd2+ions, ABCCs are identified to transport the conjugates of Cd-PCs (Zhang
et al., 2018). In Arabidopsis, 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). In addition to ABCCs, some
members from the other subfamilies of ABC transporters have been found
to confer Cd tolerance as well. AtABCG36/AtPDR8, a member of the
pleiotropic drug resistance (PDR) subfamily of ABC transporters in
Arabidopsis, is proposed to have a role in resistance to Cd by pumping
Cd2+ or Cd conjugates 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
resistance 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 CAXs are calcium (Ca2+)
specific. However, two CXAs identified in Arabidopsis, AtCAX1 and
AtCAX2, have been demonstrated to be capable of pumping not only
Ca2+ but also other cations like
Cd2+, Zn2+ and
Mn2+ into the vacuoles (Korenkov et al., 2007;
Korenkov et al., 2009).
A
later report has shown that the ectopic expression of AtCAX1 in
Petunia can significantly increase Cd tolerance and accumulation (Wu et
al., 2010).
In
the Cd hyperaccumulator A. halleri ,
Cd
tolerance was shown to be highly associated with the expression ofAhCAX1 (Baliardini et al., 2015), suggesting an involvement of
AhCAX1 in conferring Cd tolerance in this plant. A CAX2-like protein in
the hyperaccumulator S. alfredii , SaCAX2, endows 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 to the plasma membrane 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). The knockdown of OsLCT1 can lead to a
reduction up to 50% of grain Cd in rice plants grown in Cd contaminated
soil, s 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 Japonicarice . Luo et al. (2018) have also 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+, as evidenced by the
significant suppression of Cd2+ influxes by the
application of putative calcium channel inhibitors (Perfus-Barbeoch et
al., 2002; L.Z. Li et al., 2012; Chen et al., 2018).
However,
the function 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 Cd influx and uptake by root cells (Chen et al.,
2018), suggesting the possibility to identify the candidate channels
responsible for Cd transport from these two families.
4 | EVOLUTION OF CADMIUM ACCUMULATION IN
PLANTS
4.1 | Phylogenetic variation in Cd accumulation
in plants
Phylogenetic 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 there is no evidence showing Cd
is necessary for growth of algae, they have the ability to concentrate
Cd from the environments, with a manner of algae species dependent
(Klimmek et al., 2001). In fresh water green algae, such asScenedesmus spp. and Spirogyra spp. , 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, such as Ecklonia radiate , Macrocystis
pyrifera , Laminaria digitata and Sargassum spp. 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 high capacity of
Cd2+ adsorption for these marine brown algae would be
explained by the high abundance of alginate in cell wall matrix, which
is a biopolymer segment and has 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 algaePseudokirchneriella
subcapitata , the intracellular flux of Cd is at least 20 times higher
at pH 7.0 than at pH 5.0 (Vigneault and Campbell, 2005). Similar result
has been observed in Scenedesmus obliquus , with the highest value
of Cd absorption occurring at pH7.0 (Monteiro et al, 2009).
Nevertheless, for the marine brown algae Ecklonia radiate there
was appreciable Cd uptake at the pH range of 2.0-6.0 and 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 phyla: the liverworts (Marchantiophyta), mosses (Bryophyta),
and hornworts (Anthocerophyta) (Shaw et al. 2011). It has been
demonstrated that both mosses and liverworts possess the ability to
absorb heavy metal ions over the entire plant surface, due to the lack
of the cuticle layer, pronounced ion-exchange properties 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 strongly
dependent on the environmental conditions. Vukojević et al. (2005)
reported that two moss species, Bryum capillare andCeratodon purpureus , could accumulate up to 0.1% DW of Cd
(appx.1125-1250 mg/kg) in their shoots. In a later research on the other
two moss species Fabriona ciliaris and Leskea angustata ,
however, their Cd concentrations only varies from <0.1 to
7.3 mg/kg, with an average value of 1.3 mg/kg in the rainy season
(Macedo‑Miranda et al., 2016). The authors also found that Cd is
enriched much higher in the rainy season than in dry-cold season.
Furthermore, Wells and Brown (1990) found that in the mossRhytidiadelphus squarrosus lowering of 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.
Angiosperms, appeared during the Early Cretaceous period and within
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 Viridiplantae,
including five major groups: Eudicots, Monocots, Magnoliids,
Chloranthales, and Ceratophyllales (Yang et al., 2020). Angiosperms
inhabit all seven continents, as well as the oceans. They 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 has been 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,
and found 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 reported as Cd hyperaccumulators (summarized in 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, but mainly belong to the families of
Brassicaceae
and Asteraceae. Two Brassicaceae species, A. halleri and T.
caerulescens , which are the most intensively studied species of Cd
hyperaccumulating plants, also display an extraordinary ecotypic
variation in Cd accumulation (Reeves et al., 2018; Verbruggen et al.,
2013). Likewise, the Cd hyperaccumulator S. alfredii also exhibit
the fixed ecotypic differences in Cd sequestration and translocation
(Cappa and Pilon‑Smits, 2014; Reeves et al., 2018), indicative of local
adaptation of these species to the natural habitat
(Reeves
et al., 2018), or probably to the appearance of anthropogenic metal
pollution (Sobczyk et al., 2017).
Taken together, plants, especially angiosperms, display a wide
adaptation over the plant phylogeny to the presence of Cd in the
environment. 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). Similar
convergent
patterns of evaluation 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
hyperaccumulation trait in some plant species like A. halleri ,T. caerulescens and S. 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 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 between A. halleri and A.
lyrata suggests that ecological differentiation may have occurred at
the onset of speciation in this species pair (∼5 Mya,
Koch
et al., 2000) and A. 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). The other hypotheses
proposed on the selective factors of Cd accumulation by plants include:
protection against herbivores or pathogens, allelopathy and positive
physiology effect (reviewed by Cappa and Pilon-Smits, 2014).
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
plant, 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. A comparative genomics analysis of
seven Cd transporter gene families was performed 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 search for YS1-like proteins in the genome sequences of
green alga Chlamydomonas reinhardtii and red algaCyanidioschizon merolae , but could not 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
there is lack of CAX (in Cyanidioschyzon merolae andMesotaenium endlicherianum ) and ZIP (in Porphyra
yezoenesis and Volvox carteri ) homologs in several algae
species (Table 2). As been
recognized 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
Viridiplantae species, 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 (arised through unequal crossing
over) (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 an early evolution in Viridiplantae. While the
angiosperms cluster can be grouped into two subclusters 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 A. trichopoda , which is dating 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 Viridiplantae 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. Eachcluster
can be further divided into three subclusters; the subclusters in
cluster 2 are deep-branching, while those in cluster 1 are not. In the
three subclusters 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, including both
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.
5 | CONCLUSIONS AND
PERSPECTIVES
Cadmium is one of the most hazardous toxic heavy metals in the
environments, posing great risks to human health. In soil-plant system,
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 Viridiplantae 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 Viridiplantae 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 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 phylogenetic clusters showed
rampant intermixing have occurred for the orthologues of OsNRAMP5,
indicating the horizontal gene transfer involved its evolution. All
these evolutionary patterns may provide an adaptive advantage for
colonization of plants to new habitat like metalliferous soil.
Because
of lacking the 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, 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).
Table 1 The identified transporters mediating Cd uptake,
translocation, sequestration and distribution in plants sequestration
and distribution in plants