Abstract
Plant transporters are crucial for nutrient acquisition, cellular homeostasis, and stress responses. They mediate the exchange of chemicals and signals inside and outside the biomembrane in plants. Therefore, the study of plant transporters is critical to understanding the mechanisms of plant stress tolerance, moreover, transporters have potential applications in crop breeding for improved stress tolerance. Here we review recent findings about different transporters family (ABC, MATE, NRAMP, KUP, COPT/Ctr, NPF, NRT, PHT, YSL, ZIP, STP, etc.), including their roles in abiotic stress tolerance, and plant growth and yield. Moreover, we highlight the roles of transporters in plant responses to abiotic stresses such as drought, waterlogging, salt and alkali, heavy metal stress, and nutrient deficiency. To clarify the mechanisms underlying the roles of transporters in various stress responses, we integrate information about transporter activity in plants under stress and thus reveal a link between nutrient accumulation and stress tolerance. Finally, we list genes with potential applications in genetic improvement of resistrance genes, and summarize and discuss these transporters for benefiting the research community.
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Introduction
Abiotic stresses such as drought and waterlogging, soil salinization and alkalization, heavy metal toxicity, and nutrient deficiency restrict crop yields and biomass production worldwide (Vahdati and Leslie 2013). Molecular biological studies have provided extensive evidence about the mechanisms of stress tolerance in plants, including the various signaling and transcription factors involved. Intriguingly. Transporters have vital roles in plant stress responses (Hirayama and Shinozaki 2010). Transporters are a class of membrane proteins that transport biomolecules across membranes. Numerous transporters help plants move metabolites, toxic pollutants, and nutrients during growth, and these transporters, especially nutritional transporters that transfer nutrients needed for plants growth are crucial for nutrient acquisition, development, cellular homeostasis, and stress responses (Bo et al. 2017). For example, carbohydrate transporters improve tolerance to drought (Ma et al. 2019a) and waterlogging stress (Phukan et al. 2018) by adjusting carbohydrates content. Mineral nutrition transporters respond to nutrient deficiencies by regulating the Macro-elements and Micro-elements in the cytoplasm, vacuoles and extracellular space (Li et al. 2019). Metal cation transporters can adjust the ion balance in the cells to achieve the effect of anti-salt (Chai et al. 2020) and anti-metal toxicity (Veraestrella et al. 2017). Recently, there have been many research results showing that transporters are closely related to plant stress resistance, growth and development. In this review, we summarize our current understanding of the roles of different transporters in plant stress responses and examine the link between transporter activities, nutrient acquisition, and stress tolerance.
Transporters in abiotic stress tolerance
Drought tolerance
Drought stress is one of the most important factors restricting plant growth. Plants respond to drought stress by closing their stomata, causing downstream metabolic perturbations (i.e. increased activity in the photorespiration pathway) that increase reactive oxygen production (Fang and Xiong 2014). In addition, plant hormones such as abscisic acid (ABA) activate various stress responses and the plant initiates root development (Fang and Xiong 2014).
Functional studies have verified the roles of many transporters in drought stress. For example, some sugar transporters allow cells to accumulate sugar and this change in osmotic pressure increases drought tolerance. For instance, in micropropagated apple plants (Malus × domestica), increased sorbitol transporter gene (MdSOT3 and MdSOT5) activity improved drought tolerance (Li et al. 2012). Also in apple, the sucrose transporter MdSUT2.2 is phosphorylated by the protein kinase MdCIPK22, which regulates its transcription activity under drought conditions, allowing cells to accumulate sugar and thus increasing drought tolerance (Ma et al. 2019a). Movement of sodium and potassium ions also helps alleviate drought stress by affecting the osmotic balance. For example, overexpressing the rice (Oryza sativa) high-affinity potassium transporter gene OsHAK1 enhanced drought tolerance and improved grain yield under drought conditions (Chen et al. 2017a).
The stress hormone abscisic acid (ABA) plays a key role in drought tolerance. When plants sense drought conditions, ABA functions as a long-distance signal to transmit information from the roots to the above-ground tissues of the plants. The ABA signal increases drought tolerance by inducing stomata to close, maintaining water balance in cells, and increasing root permeability to water (Zhang et al. 2006). Loss-of-function Arabidopsis thaliana mutants of a plasma membrane ABA uptake transporter, ABCG40, showed reduced sensitivity to ABA and reduced resistance to drought stress (Kang et al. 2010). Overexpressing the cell membrane ABA transporter gene AtABCG25 enhanced plant drought tolerance (Kuromori et al. 2016).
Controlling the movement of guard cells enhances drought tolerance in plants by decreasing water loss and many different transporters take part in this process, including auxin, nitrate, and ABA transporters (Jarzyniak and Michal 2014). In Arabidopsis thaliana, the Major Facilitator Superfamily transporter ZINC-INDUCED FACILITATOR-LIKE 1 (ZIFL1) affects polar auxin transport, but ZIFL1.3, a truncated form produced by alternative splicing, regulates stomatal closure to mediate drought tolerance (Remy et al. 2013). The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening in Arabidopsis under drought stress (Guo et al. 2003). The Arabidopsis ABC transporter MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN5 (AtMRP5) is an important component of guard cell function and water use (Klein et al. 2003). Mutation of AtMRP4, an ABC transporter, decreased stomatal opening and increased drought resistance in Arabidopsis (Klein et al. 2004). Arabidopsis mutants of AtDTX50, a DTX/MATE (Multidrug and Toxic Compound Extrusion) family member and ABA efflux transporter, showed lower stomatal conductance and were more tolerant to drought stress than the wild type (Zhang et al. 2014). A mutant of AtABCG22, an Arabidopsis ABC transporter, had increased water loss and lower leaf temperature than the wild type due to effects on stomatal regulation (Kuromori et al. 2011). The ABC transporter AtABCB14 regulates stomatal movement by affecting malate transport and increasing osmotic pressure in Arabidopsis (Lee et al. 2008). Lastly, REDUCED CULM NUMBER 1/OsABCG5, a half-size ABC subfamily G protein, is indispensable for stomatal closure and reducing water loss in rice (Oryza sativa) (Matsuda et al. 2016).
Many stress-related transporters have been isolated by mutant analysis. Now, various “omics” techniques have been effectively used to search for anti-stress factors in plants and have uncovered the roles of various transporters in stress tolerance. For example, a whole-genome oligomer microarray analysis identified several transporter genes as significantly responsive to drought stress in rice (Oryza sativa) (Junli et al. 2007). A recent study used genome-wide sequencing data to find new transporter genes related to drought tolerance in Populus (Bai et al. 2019). Solexa sequencing and qRT-PCR identified various transporter genes that were highly expressed in drought-treated Paulownia fortunei leaves (Dong et al. 2014). The regulation of different transporter genes also plays a role in the drought tolerance of Gossypium herbaceum, as revealed using microarray analysis, pyrosequencing, and qRT-PCR of roots (Ranjan et al. 2012). A putative ATP-binding cassette (ABC) transporter ATP-binding protein was identified by proteomic analysis of proteins extracted from Hippophae rhamnoides leaves (Xu et al. 2009). Nine rice ABC transporter genes that are significantly regulated by drought stress were discovered by analysis of anatomical data analysis and qRT-PCR (Nguyen et al. 2014). With the development of sequencing technologies, omics approaches will find more and more new transporters and improve our understanding of the mechanisms by which transporters respond to drought stress.
Waterlogging tolerance
Waterlogging induces hypoxia in plants. Anaerobic respiration caused by waterlogging leads to excessive reduction of the photosynthetic electron transport chain and the formation of reactive oxygen species (ROS) such as superoxide radicals and singlet oxygen (Blokhina et al. 2003). Initially, ROS and NO production can help adaptive responses such as formation of aerenchyma and adventitious roots, but excessive ROS cause severe oxidative damage under waterlogging stress (Planchet and Kaiser 2006; Steffens et al. 2012). Transporters also take part in the waterlogging stress response in plants. AtSWEET10, a SWEET transporter, is involved in enhancing carbohydrate availability and waterlogging tolerance in Arabidopsis. AtSWEET10 expression is activated by waterlogging due to the presence of a drought-responsive element (DRE) and a GCC box in the AtSWEET10 promoter. Heterologous expression assays showed that the AtSWEET10 DRE can be targeted by MaRAP2-4, a waterlogging-responsive ERF from Mentha arvenis (Phukan et al. 2018). ABC transporter subfamily G (ABCG) gene ABCG5 is highly expressed in seedling cotyledons, and under waterlogging condition, its activity is required to form the dense cuticle to resist waterlogging damage for the normal growth of plants (Lee et al. 2020).
Salt and alkali tolerance
Soil salinization and alkalization are major environmental hazards that limit plant growth and development. Exposure to salt affects plant water relations, inducing responses similar to those of drought stress. Moreover, high salt creates ionic stress, in which excess ions (Na+) disrupt cellular metabolism. Alkali stress affects many metabolic and physiological processes, such as photosynthesis, cell ionic balance, antioxidant systems, and osmotic absorption of water (Zhang and Mu 2010). In recent years, many genes related to salt stress have been discovered, and the molecular mechanism of salt stress has been gradually elucidated (Yang and Guo 2018). In addition to the harm caused by water stress, soil salinization and alkalization also directly affect plant growth and development.
Maintaining the proper balance of sodium and potassium is an effective strategy used by plants to survive salt stress (Ali et al. 2018). Indeed, transcriptomics approaches have identified various monovalent cation transporters that function in plant responses to salinity stress. The barley (Hordeum vulgare) sodium transporter and high-affinity potassium transporter HvHKT1;1 reduces Na+ accumulation in shoots and regulates ion concentrations in root cells, thereby improving salt tolerance (Yong et al. 2018). The sodium transporter HKT1;2 plays important roles in maintaining sodium/potassium homeostasis and salt tolerance in tomato (Solanum lycopersicum) (Noelia et al. 2017). The High-Affinity Potassium Transporter EpHKT1;2 in the halophyte Eutrema parvula is a key contributor to the halophyte features of this plant and helps determine its tolerance to Na+ ion toxicity (Ali et al. 2018).
The SOS (salt overly sensitive) pathway is induced by high salt upregulates transporters such as the high-affinity potassium transporter AtHKT1;1 in Arabidopsis to regulate ion homeostasis and thus enhance plant salt tolerance (Oh et al. 2009). The Na+/H+ transporter SOS1 and the protein kinase SOS2 act with the plasma membrane transporter PUT3 and affect its regulatory activity, thereby maintaining the balance of Na+ and K+ in the cell and affecting salt resistance in Arabidopsis (Chai et al. 2020).
Other transporters, including magnesium (Mg), ammonium and sucrose transporters, also affect salt tolerance. For example, the Mg transporter OsMGT1 transports Mg2+ in the root maturation zone and enhances OsHKT1;5 activity to restrict Na+ accumulation and improve salt tolerance in rice (Zhi et al. 2017). Heterologous overexpression of the Puccinellia tenuiflora ammonium transporter PutAMT1;1 in Arabidopsis thaliana can alleviate the ammonia toxicity induced by salt stress, thus improving the root salt tolerance in the later stage of seed germination (Bu et al. 2019). Overexpressing the sucrose transporter gene MdSUT2.2 enhanced salt tolerance in a MdCIPK13 phosphorylation-dependent manner in transgenic apple (Ma et al. 2019b). OsLCT1, a low-affinity cation transporter, affects salinity tolerance in rice (Nio et al. 2018).
Transporters in multiple plant abiotic stress responses
Stresses often occur together (for example, drought and heat) and transporters take part in multiple plant stress responses. The barley silicon transporters HvLsi1 and HvLsi2 regulate Si accumulation of the shoots of barley plants under K deficiency, thereby improving osmotic stress tolerance (Seyed et al. 2017). Overexpressing AtABCG36/AtPDR8, encoding an ABC transporter, increased drought and salt-stress resistance in Arabidopsis (Kim et al. 2010). In the monocot sorghum (Sorghum bicolor), the auxin influx carriers Auxin resistant 1/like aux1 (AUX⁄ LAX) and the auxin efflux carriers Pin-formed (PIN) and P-glycoprotein (PGP) are auxin transporters that function in plant responses to ABA, salt, and drought stress (Shen et al. 2010). ProT2 is a proline transporter involved in water and salt stress responses in Arabidopsis (Rentsch et al. 1996). In cucumber (Cucumis sativus), CsTST1 functions in responses to various abiotic stresses (cold, salt, and osmotic stress), and in response to the stress hormone ABA by affecting the distribution of carbohydrates (Huang et al. 2020).
Sucrose plays a key role in regulating guard cell movement, which affects gas exchange and water loss (Antunes et al. 2017). Heterologous overexpression of a rice monosaccharide transporter gene OsMST6 may increase soluble sugar content and osmotic pressure in cells, and enhance the drought and salt tolerance in Arabidopsis (Monfared et al. 2020). Heterologous overexpression of the Dianthus spiculifolius sugar transporter genes DsSWEET17 and DsSWEET12 in Arabidopsis increased root length and fresh weight and enhanced salt, osmotic, and oxidative stress tolerance (Zhou et al. 2018a; Zhou et al. 2018b). OsSUT2, a sucrose transporter identified in rice (Oryza sativa L. cv. Nipponbare), is essential for plant tolerance to drought and salinity stress (Ibraheem et al. 2011). Arabidopsis TONOPLAST MONOSACCHARIDE TRANSPORTER1 is required for cytosolic glucose homeostasis and plays an important role in stress responses (Wormit et al. 2006). Monosaccharide-facilitated diffusion transporters affect sugar accumulation in plant cells and help regulate osmotic pressure (Yamada et al. 2010). The sucrose transporters AtSUC2 and AtSUC4 play important roles in abiotic stress tolerance in Arabidopsis via an ABA-dependent pathway (Gong et al. 2015). Many sulfate transporters take part in drought and salinity tolerance in Arabidopsis and Medicago truncatula (Gallardo et al. 2014). Using these transporters to enhance plant resistance to salt and alkali stress will be useful in plant genetics and breeding for crop improvement.
Heavy metal stress
Heavy metal toxicity has become an increasingly serious problem due to human activity, which has increased soil heavy metals such as aluminum, cadmium, manganese, and cesium (Mohammed et al. 2011). Heavy metal hyperaccumulation and tolerance are important protective mechanisms used by plants to sequester toxic metal ions and thus improve plant survival. In tobacco (Nicotiana tabacum), metal ions are isolated into vacuoles by using transporters and exchanging with H+, and thus have roles in heavy metal hyperaccumulation and tolerance (Veraestrella et al. 2017). Therefore, transporters play important roles in plant responses to heavy metal stress.
Aluminum detoxification
Aluminum (Al) toxicity inhibits root elongation and plant productivity in acidic soils. The release of organic acids from roots is an effective method used by plants to alleviate Al toxicity, a process primarily regulated by transporters (Park et al. 2017). STAR1 and STAR2 form a bacterial-type ABC transporter complex with UDP-glucose transport activity that is required for the detoxification of Al in rice (Huang et al. 2009). The expression of the ABC transporter-like gene ALUMINUM SENSITIVE3 (ALS3) increases under high Al concentrations (above the toxicity threshold) in buckwheat (Fagopyrum esculentum), and ALS3 might promote Al detoxification (Reynallorens et al. 2015).
MATE transporters take up iron by secreting primary metabolites such as citric acid into the xylem and rhizosphere. Similarly, some MATE transporters are highly expressed in root tips and secrete citric acid to improve aluminum tolerance. The rice bean (Vigna umbellata) citrate transporters VuMATE2 and VuMATE1 function in tandem to induce citrate secretion, thereby enhancing Al resistance (Liu et al. 2018b). The organic acids combine with metal ions to form stable, non-toxic complexes responsible for transport, redistribution, or reduction of metal toxicity (Upadhyay et al. 2019; Magalhaes et al. 2007). An insertion in the rice citrate efflux transporter gene OsFRDL4 increased its promoter activity and improved its expression, thereby enhancing Al tolerance (Yokosho et al. 2016). Heterologous overexpression of a Brachypodium distachyon MATE gene enhanced Al tolerance in Setaria viridis (Ribeiro et al. 2017). Genome-wide analysis of MATE family genes in poplar (Populus) and soybean (Glycine max) confirmed their function in enhancing Al tolerance (Li et al. 2017b; Liu et al. 2016a); their homologs play similar roles in bread wheat (Triticum aestivum L.) (Garciaoliveira et al. 2018).
Like citrate, malate can combine with Al to reduce its toxicity by facilitating its transport. Heterologous expression of the Brassica oleracea ALMT gene BoALMT1 increased malate secretion and H+ efflux, thereby enhancing Al tolerance in Xenopus oocytes and Arabidopsis (Zhang et al. 2018b). Al retained in the root cell walls of plants is toxic, but this can be relieved by NIP1;2-induced accelerated Al-malate transport (Wang et al. 2018a). Overexpressing the plasma membrane-located organic acid transporter gene CsALMT1 increased malate secretion and improved Al tolerance in Camelina sativa L. (Park et al. 2017). Overexpressing Al-ACTIVATED MALATE TRANSPORTER9 (Sl-ALMT9), which is regulated by Sl-WRKY42, promoted malate accumulation in tomato (Solanum lycopersicum) fruit and enhanced Al tolerance (Ye et al. 2017).
Other transporters, including those that transport Al3+ or other ions, also affect Al tolerance. The rice NRAMP (natural resistance and macrophage protein) Al transporter (NRAT1) enhanced Al resistance in transgenic Arabidopsis by transporting Al from the root cell wall to the root cell for sequestration in the vacuole (Li et al. 2014). The absence of ZmPGP1, encoding an auxin efflux carrier P-glycoprotein belonging to the ABC transporter family, led to the accumulation of high levels of auxin and alleviated Al toxicity in maize (Zhang et al. 2018c). Tobacco (Nicotiana tabacum L.) NtSUT1, a plasma membrane-localized sucrose/H+ symporter, actively regulates sucrose uptake in the root apex, promotes root elongation, and enhances Al tolerance (Kariya et al. 2017). Heterologous overexpression of the Jerusalem artichoke (Helianthus tuberosus) NHX-type transporters HtNHX1 and HtNHX2 regulate K+/H+ fluxes and cell wall structure, thereby enhancing Al3+ tolerance in rice (Li et al. 2020).
Cadmium detoxification
Cadmium (Cd) is a toxic heavy metal that affects plant growth and development due to its effects on plant nutrient absorption and other physiological processes (Clarkson 1996). Cd transporters play important roles in resistance to Cd toxicity. Genome-wide analysis of mulberry (Morus sp.) revealed four transporter families with Cd transport activity, including zinc-regulated transporters, iron-regulated transporter-like proteins (ZIPs), NRAMPs, the heavy metal ATPases (HMAs), and the metal tolerance or transporter proteins (MTPs) families; perhaps these transporters could be exploited for Cd phytoremediation (Fan et al. 2018). Negative regulation of Cd absorption via inhibiting the activity of the Fe2+ transporter IRT1 improved Cd tolerance of plants (Guan et al. 2019; Xu et al. 2018).
Bioinformatics and high-throughput sequencing identified 84 differentially expressed ABC genes in Brassica napus that are responsive to Cd (Zhang et al. 2018d). Heterologous overexpression of the Miscanthus sacchariflorus yellow stripe-like transporter gene MsYSL1 in Arabidopsis enhanced plant resistance to Cd by mediating the reallocation of metal ions (Chen et al. 2018). AtABCC3, an ABC-type transporter whose expression is induced by Cd exposure, increases phytochelatin-mediated Cd tolerance in coordination with AtABCC1/AtABCC2 (Brunetti et al. 2015). Arabidopsis OLIGOPEPTIDE TRANSPORTER3, a phloem-specific iron transporter, facilitates iron recirculation from mature to developing tissues (Zhai et al. 2014). NRT1.8, a member of the nitrate transporter (NRT1) family, removes nitrate from xylem vessels and improves Cd2+ tolerance in Arabidopsis (Li et al. 2010). In rice, OsABCG36, a G-type ATP-binding cassette transporter, does not affect the accumulation of Cd in shoots, but it exports Cd or Cd conjugates from root cells to increase plant resistance to this heavy metal (Fu et al. 2019).
Manganese detoxification
Manganese (Mn) is an important cofactor for many antioxidant defense enzymes that take part in the disposal of superoxide radicals, a function that is critical for plant survival. However, high concentrations of Mn in acidic or insufficiently drained soil are toxic to plants. NRAMP2, a divalent metal transporter of the NRAMP family, is critical for plant photosynthesis and cellular redox homeostasis in Arabidopsis (Alejandro et al. 2017). NRAMP2 plays an important role in remobilization of Mn in the Golgi to facilitate root growth under Mn-deficient conditions (Gao et al. 2017). HAK/K+ uptake (KUP)/K+ transporters (KTs) also play important roles in responses to K+ deficiency and abiotic stress in pear seedling rootstock (Yan et al. 2018).The tonoplast-localized transporter MTP8.2 (Mn-CDF metal tolerance protein) enhances plant tolerance to Mn along with MTP8.1 by sequestering Mn in plant vacuoles of root and shoot (Takemoto et al. 2017). The membrane protein CHLOROPLAST MANGANESE TRANSPORTER1 (CMT1) plays important roles in maintaining Mn homeostasis in Arabidopsis chloroplasts (Eisenhut et al. 2018). NH4+ downregulates the expression of the Mn influx transporter gene OsNRAMP5 through rhizosphere acidification, thereby improving manganese detoxification in rice (Hu et al. 2019).
Cesium detoxification
The release of cesium into the environment has led to serious environmental concerns, because it can be taken up by crops and affect crop production. Knocking out of OsHAK1, encoding a potassium transporter, reduced cesium levels in rice without affecting potassium absorption or crop yields (Rai et al. 2017). K+ UPTAKE PERMEASE (KUP) family proteins significantly reduce the accumulation of cesium in Arabidopsis; these KUP transporters play complementary rather than redundant roles in this process (Adams et al. 2019).
Resistance to many types of heavy metal stress
Metal transporters play critical roles in maintaining metal homeostasis and reducing metal toxicity. TpNRAMP5, a metal transporter isolated from dwarf Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co, and Mn but not Zn or Fe (Peng et al. 2018). Heterologous expression of SnYSL3, encoding a YSL transporter from Solanum nigrum, led to the formation of a range of metal-nicotianamine complexes to improve metal stress resistance in Arabidopsis, especially resistance to Cd and Fe (Feng et al. 2017b). NcZNT1, a Zn transporter from Noccaea caerulescens, enhanced Zn and Cd tolerance when expressed in Arabidopsis (Lin et al. 2016). Many regulators affect the expression of transporter genes, such as the post-transcriptional regulation of BnNRAMP1b, a vital Cd, Zn, and Mn transporter, by miR167 (Meng et al. 2017). The uptake of heavy metals in rice involves pH-dependent metal transporters such as OsNRAMP5, which affect Cd and Mn resistance in rice (Zhang et al. 2019b). As heavy metal pollution in soils around the world becomes more and more serious, plants with high tolerance to heavy metals will be more adaptable to the environment and have a higher survival rate, so study and utilization of metal transporters will become more and more important. Plants hyperaccumulating heavy metals also have potential uses in bioremediation of heavy metal pollution.
The roles of transporters in surviving nutrient deficiency
Plants require 17 essential elements and 14 minerals for growth, and these are only obtained through absorption from the environment, especially the soil (Nath and Tuteja 2016). The evolution of roots improved the adaptability of plants to the terrestrial environment and helped plants absorb nutrients from the soil. The absorption and utilization of soil nutrients are critical for plant growth and yield (Shahzad et al. 2018). Moreover, understanding nutrient transport has key implications for biofortification efforts to improve the nutrition of plant-based foods. Nutrient receptors and transporters play important roles in nutrient uptake and signaling (Nath and Tuteja 2016).
Phosphate deficiency
Phosphorus (P) is an essential nutrient for plant growth and development, functioning as a core component of nucleic acids and a key element in energy transfer (Peret et al. 2014); inorganic phosphate (Pi) from the soil is the only source of phosphorus for plants. The remodeling of root system architecture (RSA) is influenced by Pi deficiency, which is important for plant growth (Vance et al. 2003). In Arabidopsis, an ABC transporter complex composed of ALS3 and AtSTAR1 cooperates with LOW PHOSPHATE ROOT1/2 (LPR1/2) to regulate Pi-deficiency responses and the active remodeling of RSA by modulating Fe homeostasis (Dong et al. 2017).
The phosphate transporter 1 (PHT1) transporter family plays a major role in the uptake of phosphate from soils in plants (Nussaume et al. 2011). Heterologous expression experiments have been used to examine transporter function and establish a foundation for improving P uptake in crops, thereby reducing the need for fertilizer. For example, the rice myeloblastosis (MYB) transcription factor OsMYB5P triggers the expression of AtPht1;3 to improve phosphate acquisition and regulate shoot development and RSA (Yang et al. 2018b). The Pteris vittata phosphate transporter PvPht1;2 enhances phosphorus accumulation without inducing the uptake of the toxic element arsenic when expressed in tobacco (Cao et al. 2018). Heterologous overexpression of the rice Pi transporter gene OsPT8 increased Pi concentrations and selenium accumulation in tobacco, paving the way for breeding selenium-enriched plants (Song et al. 2017).
Plants increase Pi uptake via symbiosis with mycorrhizal fungi, which receive fixed carbon from the plant in a mutually beneficial symbiotic relationship that improves the nutrient absorption capacity of the plants and alleviates abiotic stress. Mycorrhizal fungi induce expression of some Pi transporters to improve the Pi level of the host plant, and induce some transporters to maintain the mycorrhizal fungus–plant symbiotic relationship (Maclean et al. 2017). In maize, mycorrhiza formation induces the expression of the Pi transporter gene ZmPt9 to enhance plant Pi uptake (Liu et al. 2018a). The expression of the Pi transporter gene HcPT2 from the mushroom-forming fungus Hebeloma cylindrosporum is induced by the host plant and enhances the accumulation of Pi in both the mycelium and host plant (Becquer et al. 2018).
AtNPF (nitrate transporter 1/peptide transporter family) 7.3/AtNRT1.5 is a nitrate transporter that plays an important role in regulating the response to phosphorus deficiency in Arabidopsis (Cui et al. 2019). An ABC transporter complex formed by ALS3 and NAP3 plays a critical role in the sugar-dependent response of Arabidopsis to phosphate deficiency (Belal et al. 2015). Remodeling of RSA is an effective way to enhance plant tolerance of phosphate (Pi) deficiency, which can be improved by increasing the level of the ABC transporter complex encoded by ALS3, LOW PHOSPHATE ROOT1 (LPR1), and LPR2 (Dong et al. 2017). The PHT family protein PHT5 in the vacuolar membrane regulates cytoplasmic Pi homeostasis to enhance plant growth under Pi deficiency (Lin et al. 2018; Liu et al. 2016b). Finally, VACUOLAR PHOSPHATE TRANSPORTER1 (VPT1) functions in vacuolar Pi storage and Pi adaptation in Arabidopsis (Liu et al. 2015).
Iron deficiency
Iron (Fe) is an important micronutrient for plant growth and essential metabolic processes. Fe is involved in plant photosynthesis, respiration, nitrogen fixation, plant hormone and DNA biosynthesis (Briat 2005), and Fe transporters are very important in regulating iron homeostasis to adapt to different plant growth requirements and to cope with environmental changes (Conte and Walker 2011). The NRAMP family is also involved in iron transport. In the case of iron deficiency, AtNRAMP3 regulates metal transport in the vacuole, resulting in the accumulation of Mn, Zn, and Fe in Arabidopsis (Thomine et al. 2003). The proton-coupled metal ion transporter AtNRAMP6 may be involved in the transport of Fe2+ from the Golgi/trans-Golgi network to the cytoplasm, contributing to the homeostasis and reuse of Fe2+; and mutation of AtNRAMP6 inhibits lateral root growth under iron-deficient conditions in Arabidopsis (Li et al. 2019). The iron transporter OsIRT1 can effectively take up Fe from the soil under iron deficiency conditions in rice (Bughio et al. 2002). Heterologously expressed HvYS1 (a barley yellow stripe 1 Fe transporter) increased Fe uptake, Fe translocation from root to shoot, and Fe accumulation in rice seeds (Banakar et al. 2016). Increasing iron transport in endosperm by overexpressing the vacuolar iron transporter gene TaVIT2 improved iron homeostasis in wheat tissue (Connorton et al. 2017).
Potassium deficiency
Potassium (K+) is a major nutrient that plays important roles in plant responses to osmotic stress and basic plant metabolism. Potassium is involved in photosynthesis, protein synthesis, osmotic pressure regulation, stomatal movement, enzyme activity activation, and other physiological activities in plants; it plays an especially important role in plant stress tolerance (Leigh and Jones 1984). Potassium transporters are responsible for the uptake and transport of K+. OsHAK1 (Chen et al. 2015) and OsHAK5 (Yang et al. 2014) are important high-affinity K+ (HAK) transporters that are activated under K+ deficiency conditions. Heterologous expression of ApKUP3, a high-affinity K+ transporter gene from Alternanthera philoxeroides, increased K+ accumulation and enhanced drought tolerance in rice (Song et al. 2014). The K+ transporter GhKT2 participates in K+ acquisition, transport, and distribution in cotton (Gossypium hirsutum) (Wang et al. 2018b). GhHAK5a, a high-affinity potassium transporter in cotton, is important for K+ absorption by roots in plants under potassium deficiency (Wang et al. 2019b). In maize, ZmHAK5 and ZmHAK1 regulate the dynamic balance of K+ under low K+ conditions, affecting the absorption and distribution of K+, and improving K+ utilization efficiency (Qin et al. 2019).
Magnesium deficiency
Magnesium (Mg) is an essential mineral element for plant growth and development. CorA/MRS2/MGT-type Mg2+ transporters are very important in maintaining Mg homeostasis. For instance, AtMGT6 (Mao et al. 2014) and AtMGT7 (Gebert et al. 2009) are critical for maintaining normal physiological activities in Arabidopsis under low Mg conditions. ZmMGT10 is specifically expressed in maize roots, and increased Mg2+ uptake via roots to enhance plant tolerance under magnesium deficiency conditions (Li et al. 2017a). ZmMGT12 is a Mg2+ transporter that functions in Mg transport to chloroplasts in maize (Li et al. 2018a). The Mg transporter gene OsMGT1 is required for resistance to magnesium deficiency in rice (Zhang et al. 2019a).
Copper deficiency
Copper (Cu) takes part in a variety of physiological processes in plants, making this micronutrient important for plant growth and development. Cu deficiency affects plant fertility. The main symptoms are vegetative and reproductive growth disorders, young leaf deformity, and insufficient water transport (Burkhead et al. 2009). The reported Cu transporters are mainly from the COPT/Ctr protein family. Cu might be co-transported by COPT2, COPT3, and COPT4 with COPT6. COPT7 can act alone in different tissues to regulate Cu homeostasis in rice (Yuan et al. 2011). Cu deficiency can induce the expression of the transporter genes COPT2 (in roots) and HMA1 (in leaves), causing Cu to migrate and circulate among leaves in Brassica napus (Billard et al. 2014). Other transporters also regulate Cu homeostasis, Zn transporters ZIP2 and ZIP4 can transport Cu2+ in Arabidopsis, and ZIP2 expression is significantly increased under low copper conditions (Puig et al. 2010). OsYSL16, a member of the yellow-stripe like (YSL) family and a Cu-nicotianamine (Cu-NA) transporter, is important for Cu redistribution under Cu-limited conditions in rice (Zhang et al. 2018a).
Zinc deficiency
Zinc (Zn) is an essential micronutrient for plant growth and development. In addition to promoting Zn absorption by arbuscular mycorrhizal fungi, Zn transporters are involved in Zn deficiency tolerance in plants (Khatun et al. 2018). The ZIP transporter family plays an important role in the transport of Zn. Zn deficiency can induce OsZIP6 expression in roots and leaves of rice (Kavitha et al. 2015). Under zinc-deficiency conditions, group F TabZIP transcription factors bind to ZDREs (Zn-deficiency-response elements) of TaZIP promoters to enhance TaZIP expression and maintain Zn homeostasis in wheat (Evens et al. 2017). SaZIP4 from Sedum alfredii plays critical roles in Zn accumulation, as demonstrated in transgenic Arabidopsis (Yang et al. 2018a). The tonoplast-localized transporter OsHMA3 transports Zn to and from the vacuole to help rice plants cope with Zn toxicity or the lack of Zn (Cai et al. 2019).
The roles of transporters in plant growth and yield
Transporters are responsible of the absorption of nutrients and regulate plant growth and development. Manipulating the expression of OsAAP3, encoding an amino acid transporter, increased tiller formation and grain yield in rice (Lu et al. 2018). The tomato tonoplast dicarboxylate transporter (SITDT) helps remobilize malate and citrate in the vacuoles of fruit cells, which is important for their flavor and organoleptic quality of the fruit (Liu et al. 2017b).In grape (Vitis vinifera cv. Malbec) ripening stage, ABA and GA3 increase the expression of sugar transporter genes VvHT2, VvHT3 and VvHT6 in berries to promote berry ripening (Murcia et al. 2018). The Arabidopsis jasmonate transporter AtJAT1/AtABCG16 controls the distribution of the phytohormone jasmonate and regulates plant growth and stress responses (Li et al. 2017c). The maize MATE transporter Big embryo 1 is required for the production of intermediates or products of the CYP78A pathway and regulates lateral organ initiation in plants (Suzuki et al. 2015). Transporters also link malate transport and mineral nutrition. Overexpressing OsALMT4, encoding an ALMT, affected the efflux and compartmentation of malate and increased Mn toxicity symptoms in rice (Liu et al. 2017a). Overexpressing OsNRT2.3b, encoding a nitrate transporter, promoted Pi uptake and translocation and increased grain yield in rice (Feng et al. 2017a).
Nitrogen (N) is a key factor in plant growth and root extension. Upregulating a nitrate transporter gene improved nitrogen status and plant growth in winter wheat (Triticum aestivum L.) (Jiang et al. 2017). The nitrate transporter CsNRT2.1 improves nitrate uptake, root length, and lateral root number in cucumber (Li et al. 2018b). A hexose transport protein (HT), CSHT11, plays an important role in the development of pollens and pollen tubes in cucumber (Wen et al. 2020). The ABCC3-type transporter affects seed yield and quality in chickpea (Cicer arietinum) by regulating the transport of glutathione conjugates (Basu et al. 2019). The nodule-localized Pi transporter GmPT7 enhances nitrogen fixation and seed yield in soybean (Chen et al. 2019).
The tonoplast-localized sugar transporter CITST2, whose expression is regulated by the WRKY transcription factor SUSIWM1, is involved in sugar uptake and accumulation in the flesh cells of watermelon (Citrullus lanatus) fruit (Ren et al. 2018). Expressing the human UDP-galactose transporter gene hUGT1 increased the lignin content and hardness of leaves and stems in tobacco (Abedi et al. 2018). Genome-wide identification, expression, and functional analyses demonstrated that the sugar transporter (STP) gene family is involved in early tuber growth and monosaccharide distribution in cassava (Manihot esculenta) (Liu et al. 2018c). Sucrose transporters also function in cotton fiber elongation, which can be activated by suppressing the expression of the putative sterol carrier protein gene GhSCP2D (Zhang et al. 2017).
Pollen development is key for high yields of grain/seed and fruit crops. The tapetum plays an important role in pollen development. The ABCG/WBC-type ABC transporters play a crucial role in the transport of sporopollenin precursors for exine formation on the pollen surface (Choi et al. 2011). The ABC transporter AcABCG38 plays important role in pollen development in pineapple (Ananas comosus), suggesting it could be used to improve pineapple production (Chen et al. 2017b).
Arbuscular mycorrhizal (AM) symbiosis is important for plant growth and defense due to the exchange of signals exchange between plant roots and AM fungi. Finally, the N-acetylglucosamine (GlcNAc) transporter NOPE1 stimulates fungal pathogenesis, increases the expression of virulence genes, and functions in AM symbiosis (Nadal et al. 2017). Destroying the activity of the amino acid transporter OsLHT1 inhibits the growth and reproduction of rice (Wang et al. 2019a). By using transporters that improve plant growth and yield, future research can produce higher yields and improve quality.
Summary and conclusions
In this review, we provided an overview of the roles of transporters in plants under stress conditions. We summarized these transporters in Table S1, S2 and S3 and drawn a figure about the transporters transport substances under a variety of environmental stresses (Fig. 1). In conclusion, when plants are subjected to different external pressures, transporters will take different measures to protect the plants. Under salt stress, Na+ efflux by the role of the transporters in plasma membrane, and the transporters on the vacuole membrane and the vesicle membrane will cause Na+ to flow into them, thereby reducing the Na+ concentration in the cytoplasm and avoiding the cells from being poisoned by salt ions (Yang and Guo 2018). The transporters maintains the necessary material balance in the plant cells to response to stresses. Heavy metal stress triggers the transporters to store excess heavy metals in the vacuole, and nutrient deficiency causes transporters to transport nutrients in vacuole to cytoplasm. Similarly, under stress, plants will induce transporters to transport signal molecules, which will allow the expression of some stress-resistant genes to deal with adverse environments (Fig. 1). Transporters manage the acquisition of essential macro- and micronutrients while also play essential roles in preventing damage from environmental conditions such as high salt and heavy metals. Transporter families such as ABC transporters, which function in various parts of the plant, are involved in plant growth and development and the physiological and biochemical reactions required for stress resistance (Do et al. 2018). Transporters also interact with multiple metabolic pathways or regulate key genes to enhance stress resistance in plants. Therefore, the exploration of transporters is important for understanding plant stress resistance and plant growth, and for crop improvement.
Transporters transport substances under abiotic stress. Under different abiotic stresses, transporters transport different substances to achieve ion balance or regulate the expression of stress response genes, so as to deal with the damage caused by stresses in plants
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Li, P., Luo, T., Pu, X. et al. Plant transporters: roles in stress responses and effects on growth and development. Plant Growth Regul 93, 253–266 (2021). https://doi.org/10.1007/s10725-020-00684-3
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DOI: https://doi.org/10.1007/s10725-020-00684-3