Targeting aquaporins to alleviate hazardous metal(loid)s imposed stress in plants

https://doi.org/10.1016/j.jhazmat.2020.124910Get rights and content

Highlights

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    Hazardous metals/metalloids stress cause drastic crop losses, food contamination and environmental issues.

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    Transporter proteins like aquaporins has great role under hazardous metals/metalloids stress.

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    Recent advancements in analytical tools and technics can be better explore aquaporins to make crop stress tolerant.

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    Numerous options like transgenic development are available to reduce uptake of hazardous metals/metalloids in plants.

Abstract

Uptake of hazardous metal(loid)s adversely affects plants and imposes a threat to the entire food chain. Here, the role of aquaporins (AQPs) providing tolerance against hazardous metal(loid)s in plants is discussed to provide a perspective on the present understanding, knowledge gaps, and opportunities. Plants adopt complex molecular and physiological mechanisms for better tolerance, adaptability, and survival under metal(loid)s stress. Water conservation in plants is one such primary strategies regulated by AQPs, a family of channel-forming proteins facilitating the transport of water and many other solutes. The strategy is more evident with reports suggesting differential expression of AQPs adopted by plants to cope with the heavy metal stress. In this regard, numerous studies showing enhanced tolerance against hazardous elements in plants due to AQPs activity are discussed. Consequently, present understanding of various aspects of AQPs, such as tertiary-structure, transport activity, solute-specificity, differential expression, gating mechanism, and subcellular localization, are reviewed. Similarly, various tools and techniques are discussed in detail aiming at efficient utilization of resources and knowledge to combat metal(loid)s stress. The scope of AQP transgenesis focusing on heavy metal stresses is also highlighted. The information provided here will be helpful to design efficient strategies for the development of metal(loid)s stress-tolerant crops.

Introduction

Stress imposed in plants by hazardous heavy metals and metalloids (metal(loid)s), their toxicity, and the resulting adverse effects on the food chain and the surrounding environment are still topical. Heavy metals have relatively high density, atomic number, atomic weight, and a specific gravity greater than 5.0. Naturally, heavy metals are mostly found in soil and aquatic ecosystems. Some of the heavy metals like iron (Fe), zinc (Zn), and copper (Cu) are considered essential for plants and animals since they play a significant role in physiological and biochemical functions (Wintz et al., 2002). However, metal(loid)s like lead (Pb), arsenic (As), mercury (Hg), cadmium (Cd), barium (Ba), chromium (Cr), selenium (Se), nickel (Ni), cobalt (Co), and silver (Ag) are considered toxic or poisonous even at low levels and are significant environmental pollutants. Some of these elements like As and Se have properties in between metals and non-metals and categorized as metalloids, but commonly considered as a member of heavy metals. Heavy metal (considered both metal and metalloids) stress has a negative impact on the normal functioning of plants and the environmental health of soil organisms (Bhat et al., 2019, Carrier et al., 2003, DalCorso et al., 2010, Sharma and Dubey, 2007). Crop plants growing in heavy metal polluted areas show a drastic reduction in growth and yield (Shivaraj et al., 2019, Wang et al., 2016). Anthropogenic activities such as mining, energy production, smelting operations, and agricultural activities increase heavy metal pollution. As a consequence, plants take up these element at such elevated levels where even essential elements can cause deleterious effects. The heavy metal polluted areas are increasing exponentially worldwide which is causing extensive losses in agricultural produce as well as imposing a great risk to domestic animals and human health (Ratcliffe et al., 2017, Shivaraj et al., 2020). Widespread areas in countries such as Albania and North Greece have been polluted with heavy metals like Pb, Cu, and Cd (Shallari et al., 1998, Zantopoulos et al., 1999) and Cd, Cu, and Zn in China, Japan and Indonesia (Herawati et al., 2000). Moreover, approximately 720 sites on the National Priority List (NPL) of the United States are contaminated with heavy metals (Mulligan et al., 2001). Heavy metal pollution and the accumulation of metals in soil impose many challenges for agriculture. It can adversely affect crop growth, crop productivity, food safety, and marketability. Further, accumulation of heavy metals also causes necrosis, chlorosis in younger leaves, turgor loss, crippled photosynthetic apparatus, reduction in seed germination, and reduction in growth (Carrier et al., 2003, DalCorso et al., 2010, Sharma and Dubey, 2007). Thus, contamination of agricultural soil has become a serious issue globally, and the need for understanding the mechanisms involved in heavy metal stress tolerance is therefore a subject of highest priority.

More extensive efforts using versatile approaches and tools are needed to develop novel crop varieties with better tolerance against heavy metals. Recent advances in genomics, transcriptomics, metabolomics, and proteomics have aided the identification and characterization of genes regulating heavy metal uptake, accumulation, and different molecular mechanisms providing tolerance. Such genes can be exploited for the development of heavy metal tolerant crop varieties (Singh et al., 2016).

Aquaporins (AQPs) are one of the prime candidates thought to play a critical role in heavy metal stress tolerance (Przedpelska-Wasowicz and Wierzbicka, 2011, Shivaraj et al., 2019). The prime discovery of AQPs by Peter Agre and his colleagues leads a path to study the role of AQPs in physiological processes such as biotic and abiotic stress including heavy metal stress in plants (Johansson et al., 2000, Preston and Agre, 1991, Preston et al., 1992, Tyerman et al., 1999). Aquaporins are channel forming transmembrane proteins that allow the passage of water molecules and other small solutes across the bio-membranes. Aquaporins are mostly homo-tetramers of four identical subunits, with each subunit having a typical six membrane-spanning helices (H1 - H6) intertwined with five loops (A - E). Solute transport through the AQPs is tightly regulated and has a great level of solute specificity. The selective permeability of AQPs is regulated by two constrictions which include, conserved NPA (asparagine-proline-alanine) motifs present at loop B and loop E and aromatic arginine selectivity filter (ar/R) comprises of four amino acids residues on H2, H5, LE1, and LE2. Based on the sequence similarity and the subcellular localization, the AQP family in higher plants have been further classified into five subfamilies namely, plasma membrane intrinsic proteins (PIPs), the tonoplast intrinsic proteins (TIPs), the nodulin26-like intrinsic proteins (NIPs), the small basic intrinsic proteins (SIPs) and the uncategorized intrinsic proteins (XIPs) (Chaumont et al., 2001, Johanson et al., 2001, Kaldenhoff and Fischer, 2006, Quigley et al., 2001).

In the present article, we have discussed the uptake and transport of water and other solutes by AQPs under heavy metal stress. Emphasis is given on studies suggesting a role of AQPs in improving plant resilience under stress. Defining the solute specificity, gating mechanism, transcriptional, and post-translational regulation of AQPs will provide an opportunity to make desired genetic manipulations enhancing stress tolerance. A better understanding of the AQP transport system will help to accelerate translational research required to engineer stress-tolerant crop varieties. In this regard, recent technological advancements for studying AQPs have been described in detail. In addition, efficient exploration of approaches like transgenic development and genome editing to achieve desired manipulations are discussed. The review addresses the present understanding of AQPs, knowledge gaps, and opportunities for translational research. Providing a whole picture of the different aspects of AQPs that can be utilized for the production of superior designer crops is the major objective of this review.

Section snippets

Effect of heavy metal on water uptake at root level and transport to different aerial tissues

Roots, playing major functions of the absorption of water and nutrients uptake, anchoring the plant body, are also the first site of contact for heavy metals (Barcelo et al., 1988, Becerril et al., 1989, Burkhead et al., 2009, Feleafel and Mirdad, 2013). Generally, a very minor portion of the heavy metals present in the soil is translocated to the above ground parts, even though it cause numerous phytotoxic effects in plants. Phytotoxic effects due to heavy metals on plant majorly include

Role of aquaporin under heavy metal stress

Aquaporins, a class of water channel proteins permeate major transmembrane water flow in most of the organisms including plants. Aquaporins function both by alterations in the conductivity as well as expression patterns. The conductivity of AQPs is altered in response to heavy metal stress leading to a decrease in membrane water permeability as reported in epidermal cells of Alium cepa in response to Cd, Hg, Pb, and Zn (Przedpelska-Wasowicz and Wierzbicka, 2011). The gating of AQPs starting

Advanced tools and techniques for aquaporin studies

The advancement in the computational tools and the availability of omics scale data like genomic, transcriptomic, and proteomic data enables the detailed study of AQPs in plants. Numerous computational tools and analytical pipelines are available to predict the 3D structure, conserved motifs and domains, pore structure, pore size, cavities, sub-cellular localization, phosphorylation sites, heterodimerization, expression profile, and co-expression network of AQPs (Deshmukh et al., 2016). In

Differential expression of aquaporins under heavy metal(loid) stress in plants

Numerous comparative transcriptomic studies have elaborated differential responses of AQPs under various abiotic stresses, including heavy metal stresses (Table 1). For instance, PIPs are a major class of AQPs found to be down-regulated in B. juncea plants exposed to As(III) which led to decreased water content and inhibited seedling growth (Srivastava et al., 2013). Till now very less is known about the transcriptional regulation of AQPs under Cd stress, but one report from barley roots

Metal and non-metal inhibitors of aquaporins

Various metal and non-metal ions act as inhibitors of plant AQPs and provide both detrimental as well as beneficial effects on plant growth (Table 2). Particularly mercuric chloride (HgCl2), a major inhibitor of AQPs, has been regularly used to test AQP activity in both plants and animals (Maggio and Joly, 1995). Mercuric chloride mediated inhibition of AQUA1 has been reported in poplar (Ariani et al., 2019). Many previous studies suggest that sub-millimolar concentrations of Hg or mercurial

Regulation of aquaporins gating mechanism by heavy metals

The AQP gating mechanism (opening and closing of water channels) plays a vital role in the regulation of water passage across the biomembrane. One of the pioneer studies (Törnroth-Horsefield et al., 2006) put forth comprehensive efforts to describe the high-resolution structure of plant AQP which shed light to understand the molecular gating mechanism of AQP. They disclose the X-ray structure of Spinach oleracea plasma membrane AQP (SoPIP2;1) in its open and closed conformations with a

Mechanisms involved in AQP-mediated regulation of heavy metal(loid) stresses

Efflux is one of the predominant mechanisms utilized by plants for resisting the stress imposed by hazardous metal(loid)s. Multiple reports suggest the impending importance of efflux transporters in detoxification by excreting hazardous metal(loid)s out of the cell (Singh et al., 2015, Singh et al., 2016). Many AQPs have such efflux transporter activity. The AQP involved in As(III) uptake in rice, Lsi1 (Oryza sativa NIP2:1), is also engaged in As(III) efflux (Zhao et al., 2010). In addition to

Heterologous expression of plant aquaporin showing enhanced heavy-metal resistance

Multiple instances of heterologous expression of AQPs, have been performed for functional annotations, to increase heavy metal tolerance in crops, or for phytoremediation purposes (Table 3). For functional annotations, heterologous expression in Xenopus oocytes and Saccharomyces cerevisiae are mostly preferred approaches. Heterologous expression of AtNIP1;7 in yeast acr3Δ genotype showed the increased uptake of As(III) (Isayenkov and Maathuis, 2008) confirming its role in As(III) uptake in

Identification of desired AQP alleles (allele mining) and marker-assisted breeding

Sequencing of diverse crop plants has led to the aggregation of a vast amount of information in the public domain that can be used to isolate superior alleles of genes associated with agronomically important traits. For the dissection of natural variation occurring in candidate genes, allele mining is a promising approach that can be exploited for the identification of novel haplotypes, and also in the understanding of gene evolution. Identification of novel alleles helps in the development of

Summary and future perspectives

Numerous physiological fluctuations have been reported in the plants as a consequence of heavy metal stress as discussed in the present article. Alteration in water status is one of the earliest responses in plants when subjected to heavy metal stresses. Heavy metals reduce water uptake by roots as well as affect short distance transport of water across different tissues. The heavy metals induced alterations are attributed largely to differential expression of AQPs involved in water homeostasis

CRediT authorship contribution statement

Sanskriti Vats, Sreeja Sudhakarn, Anupriya Bhardwaj: Wrote the original draft. Sanskriti Vats, Yogesh Sharma, Sreeja Sudhakarn: Contributed in Visualization. Sudhir Kumar, Humira Sonah, Tilak Raj Sharma, Rupesh Deshmukh: Conceptualized, Writing - review & editing. Rupesh Deshmukh: Supervised. All the authors read and approved the final draft.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors are thankful to the Department of Biotechnology, Government of India for the Ramalingaswami Fellowship Award to Humira Sonah and Rupesh Deshmukh; Department of Science and Technology, India for JC Bose Fellowship to Tilakraj Sharma and funding support (CRG/2019/006599) to Rupesh Deshmukh; Council of Scientific & Industrial Research (CSIR), India for granting Shyama Prasad Mukherjee Fellowship (SPMF) to Sanskriti Vats, and Junior Research Fellowship to Sreeja Sudhakarn and Yogesh

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      Citation Excerpt :

      These results strongly support that Se has beneficial effects on Na+ compartmentalization in root vacuoles under saline stress. Aquaporins function widely in ion and water uptake and are involved in heavy metal tolerance in plants (Vats et al., 2021). The transcript level of aquaporins was enhanced in M. hupehensis roots under high-salinity conditions.

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