Rupesh Deshmukh1, Durgesh Kumar Tripathi2, Henry Nguyen3 and Humira Sonah1
1National Agri-Food Biotechnology Institute (NABI), Mohali, India
2Amity Institute of Organic Agriculture (AIOA), Amity University, Uttar Pradesh, India
3Division of Plant Sciences, University of Missouri, Columbia, MO, USA
e-mails: rupesh@nabi.res.in; dktripathiau@gmail.com; nguyenhenry@missouri.edu; humira@nabi.res.in
Intra-and intercellular traffickings are crucial aspects for the growth and survival of any organism, including plants. Such communication, regulated by transporter proteins, ensures nutrient transport, senses environmental changes and generates an appropriate response. Transporter proteins play an important role in stress signal sensing by transporting a variety of molecules across the biological membrane. Subsequent plant response to the stress signal also involves several types of transporters (Vishwakarma et al. 2019). Plants have evolved hundreds of transporters with varying solute specificity and modes of regulation (Deshmukh et al. 2020). In plants, several transporter families have been studied extensively to understand the evolution of such complex regulation. In this regard, recent advances in the omics field have helped perform genome-wide studies and subsequent characterisation. For instance, a genome-wide study recently performed in flax has provided crucial information about the evolution and functionality of the Detoxification efflux carriers (DTX) gene family (Ali et al. 2021a). Similarly, about three thousand transporter proteins were predicted and subsequently studied for gene expression, co-expression network, structural diversity and allelic variation in soybean. Later the analytical workflow was used to perform a similar genome-wide characterisation in 47 diverse plant species (Deshmukh et al. 2021). Many of these recent studies have efficiently explored publicly available genomic and transcriptomic resources to perform transporter gene families’ characterisation (Deshmukh et al. 2016). Similarly, predictive tools, particularly those hosted on online servers, have also played an important role in understanding the structural and functional attributes of different transporters (Vishwakarma et al. 2019). Specialised online databases have been developed to provide extensive information on transporters identified in plant genomes (Deshmukh et al. 2021). These interactive databases will serve as a start point to identify candidate genes in loci identified through QTL (quantitative trait mapping) and GWAS (genome-wide association study) approaches.
Plants employ several different strategies, including morphological and physiological changes, to cope with nutrient deficiency. Such quick responses involved the production and transport of hormones and signalling molecules (Park et al. 2017). The role of hormones in regulating plant responses to nutrient deficiencies has been extensively studied, but very few studies have addressed the transporters involved in the process (Park et al. 2017, Al Murad et al. 2021, Bandyopadhyay and Prasad 2021). The role of transporters in sensing environmental changes and subsequent plant adaptation has been evident in several studies (Vishwakarma et al. 2019, Bandyopadhyay and Prasad 2021, Barzana et al. 2021). However, the precise regulation of complex networks of transporters is yet not well understood. Under nutrient stress, a general response like induction of plasma-membrane transporter genes, tonoplast specific transporters and down-regulation of aquaporins have been observed (Barzana et al. 2021). Leaf senescence is an important event induced due to nitrogen deficiency or as a growth stage, where the plant’s nitrogen use efficiency plays a crucial role (Beier and Kojima 2021). Under such conditions, the release of amino acids from proteins and subsequent catabolism of ammonium and urea takes place in the plant system. The translocation and conversion of metabolites involve many membrane transporters (Beier and Kojima 2021). To tackle nutrient deficiency or improve the nutrient use efficiency of crop plants, nutrient transporter and water channels (aquaporins) needs to be considered.
Being a fundamental part of the living system, transporter proteins are involved in many cellular processes defining the organism’s response. Plant transporters are known to play a significant role during host-pathogen interaction. Over the last couple of decades, efforts have highlighted the essential role of mineral nutrient transporters during symbiotic or pathogenic interaction in plants (Sun et al. 2021). Similarly, the principal water channels, aquaporins, play an important role not only in regulating the water status during host-pathogen interaction but also control the transport of small molecules like H2O2, ammonia, CO2, and metalloids (silicon, boron, germanium, etc.) (Deshmukh et al. 2017). Recently, a study performed to understand the effect of flagellin-derived peptide flg22 on aquaporin expression in Arabidopsis revealed the significant role of PIP2 (class of Aquaporin) in flg22-induced stomatal response (Cui et al. 2021). The study provides an excellent example of how transporter-mediated membrane dynamics play an important role in the physiological process leading to stomatal immunity. Sugar transport is another important activity decisive for the host-pathogen interaction. Sugar molecules are central for stress sensing, signalling and subsequent complex responses (Dayer et al. 2021, Cui et al. 2021). In plants, three classes of transporter proteins, SWEETs (Sugars Will Eventually be Exported Transporter), MSTs (Monosaccharide Transporters), and SUTs (Sucrose Transporters), perform sugar transport under stress, growth and development as well as in source to sink movement. SWEET genes have been extensively studied for their role in Bacterial blight disease in rice (Varshney et al. 2019). Pathogen-mediated activation of SWEETs genes upraises sugar flow at infection site where pathogen use it. The allelic variation for SWEET genes provides a source of resistance genes where modulated activation restricts the disease development.
The role of sugar transport is also important under abiotic stress conditions. Increased sucrose content has been observed under drought and salinity stress in many plants. In rice, OsSWEET13 and OsSWEET15 are found to regulate sucrose transport under abiotic stress conditions (Mathan et al. 2021). The expression of both these genes is thought to be regulated by abscisic acid (ABA) since the OsbZIP72 (ABA-responsive transcription factor) binding site is present in the promoter of both genes. The crosstalk of SWEET and phytohormones plays a critical role under drought (Kaur et al. 2021). Adaptive changes in plants reallocating photoassimilates under stress conditions involve complex crosstalk between a variety of transporters and phytohormones. The processes of source-sink communication in the form of transport of photoassimilates, as well as signalling molecules, ensure crop yield under stress conditions. The crop improvement programs need to explore source-sink communications to redefine the plant ideotype ensuring better yield potential.
Uptake and transport of mineral nutrients is another important function of transporter proteins. Several active and passive transporters having a role in the uptake of different elements at the root level and subsequent transport to various tissues have been identified. Aquaporins are one of such element transporters, predominantly involved in the transport of many metalloids, including beneficial elements like boron, selenium and silicon, and toxic elements like arsenic and germanium (Raina et al. 2021, Kumawat et al. 2021). Mapping of loci governing genetic variation for the accumulation of different elements is an efficient strategy to enhance the molecular understanding and explore the information for crop improvement programs. Jia et al. (2021a) have performed a genome-wide association study using a diverse set of spring barley to identify loci governing boron accumulation in grain. Subsequently, candidate gene evaluation identified HvNIP2;2/HvLsi6 as a functional boron transporter. Another significant study by Wang et al. (2021) has shown interactive regulation of boron transporters BOR1 with NO3−. Such studies indicate a complex regulation of the transporter protein in sensing the nutrient status and maintaining specific solute transport under adverse conditions. Aluminum ion concentration high levels inhibit plant growth mainly by altering the membrane potential and interfering with the role of membrane transporter proteins. The broad range of similar solutes transported by transporters makes the situation complicated under exposure to hazardous elements. The toxic level of Al3+ has been shown to affect the functionality of nitrate (NO3−), ammonium (NH4+), potassium (K+), calcium (Ca2+), and magnesium (Mg2+) transporters (Wang et al. 2021).
The transporter’s role in maintaining plant homeostasis is crucial in biotic as well as abiotic stress (Dahuja et al. 2021, Devanna et al. 2021, Kumawat et al. 2021). Under salt stress, altered cellular ionic homeostasis is one of the primary responses regulated by transporters involved in sodium, chloride, calcium and potassium transport (Basu et al. 2021). Similarly, other transporters involved in the uptake of nutritional and beneficial elements also play a role in the stress alleviation mechanism. Silicon, one of the beneficial elements for the plant, is being widely explored to combat plant stress (Berni et al. 2021). However, very little is known about the exact role of silicon. In contrast, mechanism like the Salt Overly Sensitive (SOS) pathway regulating sodium ion homeostasis is one of the highly studied areas. Several genes involved in the SOS pathways have been cloned. The available information about the genes involved in the SOS pathway facilitates the identification of homologs in several different plants, allowing the genetic variation of these genes to be used breeding approaches (Ali et al. 2021b, Berni et al. 2021, Brindha et al. 2021). Genes involved in the SOS pathway, Na+/H+ exchange (Na+/H+ exchangers) and ion transporter work systematically to alleviate the toxicity (Amin et al. 2021, Basu et al. 2021, Jia et al. 2021b). Transcription factors play an important role in coordinating appropriate response by regulating the expression of genes involved in transport, signal transduction, stress scavengers and hormonal responses (Amin et al. 2021, Jia et al. 2020b, Munsif et al. 2021).
In this special issue, several research articles describing the role of solute transporters and review articles highlighting the knowledge gaps and presenting hypotheses explaining molecular mechanisms involved in plant responses under stress conditions are compiled. The extensive information provided in the special issue will help accelerate efforts towards a better understanding of transporters and subsequent exploration of knowledge through translational research.
Focus on Mineral Transporters
Without access to mineral nutrients; such as iron (Fe), boron (B), chlorine (Cl), sulphur (S), and selenium (Se); the complex array of metabolic processes that occur in plant cells would grind to a halt. This is due to the variety of functions they contribute, ranging from the transfer of electrochemical energy across membranes, granting proteins with highly specialised enzymatic properties, and fortifying the structural building blocks of cell walls. As mineral nutrients cannot be synthesised by the cell, plants make use of their sprawling network of roots in combination with transporters that are specialised in the acquisition and subsequent transport of nutrients throughout the plant. Due to the vital role of these transporters, any interruption in their normal functioning can have disastrous results on plant health and vigour.
In this Special Issue of Physiologia Plantarum, the role of solute transporters under stress conditions in plants is being explored. For insights into the transport of mineral nutrients, read on for more here: https://bit.ly/3d8OQ8N
Focus on Abiotic stress
“No man is an island entire of itself”. Similarly, no plant can isolate itself from the relentless impact of its environment. Just as the essential activities of cellular transporters are fine-tuned by a range of signals originating from within the plant; stimuli from the plant’s environment are perceived and acted upon via cascades of signalling molecules, triggering adaptive responses in transporters to limit damage or optimise productivity. These environmental factors can take many forms, such as extremes of temperature, drought, nutrient-deficiency, or the presence of a harmful toxin – any influence in the environment that challenges the status quo of the plant. As our understanding of the impact of these abiotic stresses on plant transporters increases, so too does our capacity to bolster plant defences; with profound implications for the productivity and sustainability of crops in future climate conditions.
In this Special Issue of Physiologia Plantarum, the role of solute transporters under stress conditions in plants is being explored.
Focus on Sugars
Photosynthesis, the process of generating sugars from carbon dioxide, water, and sunlight, is one of the defining features of the Plant Kingdom and forms the foundation of almost every food web on Earth. The resulting sugars can be used directly to fuel growth, sequestered away as starch for later use, or serve as structural components in cellular architecture. A less obvious, but still vital role, is their use as signalling compounds that integrate external stimuli with the metabolic status of the plant – impacting the plant’s physiology, developmental programming, and the way it responds to stress. As a result, researchers have become increasingly interested in the transporters responsible for migrating sugars between cells and around the plant.
Focus on Plant-Microbes Interaction
Recent innovations in DNA sequencing approaches have shed light on the invisible world around us, revealing hidden communities of microorganisms that populate our bodies and our surroundings. These microbes (bacteria, archaea, fungi, protists, and viruses) lead lives that are intricately entwined with our own; with activities that range from disease-causing pathogens to essential helpers that contribute to our health and wellbeing. Similarly, plants coexist with their own complex microbial communities, commonly known as the microbiome, and must carefully regulate these interactions to optimise beneficial processes, such as enhancing water and nutrient acquisition, while safeguarding themselves from microbial assault. Central to these plant-microbe interactions are the plant transporters, which shuttle valuable mineral nutrients and sugars between the plant and its microbial helpers. These transporters are natural targets for plant pathogens, which can bypass the plants immune system and hijack the transporters for their own gain. Consequently, plant transporters are subjects of intense interest for researchers seeking to optimise crop nutrition and growth, while bolstering their defences to disease-causing pathogens.