Aquaporins are membrane channels that facilitate the transport of water and small neutral molecules across biological membranes of most living organisms. In plants, aquaporins occur as multiple isoforms reflecting a high diversity of cellular localizations, transport selectivity, and regulation properties. Plant aquaporins are localized in the plasma membrane, endoplasmic reticulum, vacuoles, plastids and, in some species, in membrane compartments interacting with symbiotic organisms. Plant aquaporins can transport various physiological substrates in addition to water. Of particular relevance for plants is the transport of dissolved gases such as carbon dioxide and ammonia or metalloids such as boron and silicon. Structure-function studies are developed to address the molecular and cellular mechanisms of plant aquaporin gating and subcellular trafficking. Phosphorylation plays a central role in these two processes. These mechanisms allow aquaporin regulation in response to signaling intermediates such as cytosolic pH and calcium, and reactive oxygen species. Combined genetic and physiological approaches are now integrating this knowledge, showing that aquaporins play key roles in hydraulic regulation in roots and leaves, during drought but also in response to stimuli as diverse as flooding, nutrient availability, temperature, or light. A general hydraulic control of plant tissue expansion by aquaporins is emerging, and their role in key developmental processes (seed germination, emergence of lateral roots) has been established. Plants with genetically altered aquaporin functions are now tested for their ability to improve plant tolerance to stresses. In conclusion, research on aquaporins delineates ever expanding fields in plant integrative biology thereby establishing their crucial role in plants.

Aquaporins in Plants.

Aquaporins are membrane channel proteins ubiquitously present in all kingdoms of life. Although aquaporins were originally discovered as water channels, their roles in the transport of small neutral solutes, gasses, and metal ions are now well established. Plants contain the largest number and greatest diversity of aquaporin homologs with diverse subcellular localization patterns, gating properties, and solute specificity. The roles of aquaporins in physiological functions throughout plant growth and development are well known. As an integral regulator of plant-water relations, they are presumed to play an important role in plant defense responses against biotic and abiotic stressors. This review highlights involvement of various aquaporin homologs in plant stress responses against a variety of environmental stresses that disturb plant cell osmotic balance and nutrient homeostasis.

The Roles of Aquaporins in Plant Stress Responses.

Arbuscular mycorrhizal (AM) fungi, which form symbioses with the roots of the most important crop species, are usually considered biofertilizers, whose exploitation could represent a promising avenue for the development in the future of a more sustainable next-generation agriculture. The best understood function in symbiosis is an improvement in plant mineral nutrient acquisition, as exchange for carbon compounds derived from the photosynthetic process: this can enhance host growth and tolerance to environmental stresses, such as water stress (WS). However, physiological and molecular mechanisms occurring in arbuscular mycorrhiza-colonized plants and directly involved in the mitigation of WS effects need to be further investigated. The main goal of this work is to verify the potential impact of AM symbiosis on the plant response to WS. To this aim, the effect of two AM fungi (Funneliformis mosseae and Rhizophagus intraradices) on tomato (Solanum lycopersicum) under the WS condition was studied. A combined approach, involving ecophysiological, morphometric, biochemical, and molecular analyses, has been used to highlight the mechanisms involved in plant response to WS during AM symbiosis. Gene expression analyses focused on a set of target genes putatively involved in the plant response to drought, and in parallel, we considered the expression changes induced by the imposed stress on a group of fungal genes playing a key role in the water-transport process. Taken together, the results show that AM symbiosis positively affects the tolerance to WS in tomato, with a different plant response depending on the AM fungi species involved.

http://www.plantphysiol.org/content/plantphysiol/early/2016/04/19/pp.16.00307.full.pdf

Insights On the Impact of Arbuscular Mycorrhizal Symbiosis On Tomato Tolerance to Water Stress

Summary
Silicon (Si), although mostly ignored by plant nutritionists and ecologists, is now gaining more attention because of its beneficial role in plant fitness under stress environment imposed by a diverse range of biotic and abiotic factors. Si appears to systematically confer benefits to plants as long as a given species can absorb the element. Here, we review recent developments regarding the molecular mechanisms, evolution, regulation and structural specificity of influx transporter proteins involved in Si uptake by plants.
Si absorption is facilitated by specific nodulin 26-like intrinsic proteins (NIPs). The Si transporter NIPs have evolved a unique amino acid selective filter (SF), which is one of the required features to regulate the influx of Si. While Si accumulation in plants requires the dual action of both an influx transporter and an efflux transporter, it appears that the presence of the former is the indispensable key for a plant to be able to absorb Si.
Based on sequence analyses and comparisons, influx transporters appear to have conserved features across all species that allow to discriminate between plants that are Si competent or not. While it is unclear how and why plants have acquired or lost this trait, genomic data now offer a reliable tool to predict with accuracy which plant species are predisposed to benefit from Si. This will undoubtedly result in a better understanding of Si role in many fundamental aspects of ecology regarding plant fitness under stress.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2435.12570

Molecular evolution of aquaporins and silicon influx in plants

In this review, we provide a brief synopsis of the evolution and functional diversity of the aquaporin gene superfamily in prokaryotic and eukaryotic organisms. Based upon the latest data, we discuss the expanding list of molecules shown to permeate the central pore of aquaporins, and the unexpected diversity of water channel genes in Archaea and Bacteria. We further provide new insight into the origin by horizontal gene transfer of plant glycerol-transporting aquaporins (NIPs), and the functional co-option and gene replacement of insect glycerol transporters. Finally, we discuss the origins of four major grades of aquaporins in Eukaryota, together with the increasing repertoires of aquaporins in vertebrates.

https://www.journals.uchicago.edu/doi/pdf/10.1086/BBLv229n1p6

Evolution and functional diversity of aquaporins.

The family of aquaporins, also called water channels or major intrinsic proteins, is characterized by six transmembrane domains that together facilitate the transport of water and a variety of low molecular weight solutes. They are found in all domains of life, but show their highest diversity in plants. Numerous studies identified aquaporins as important targets for improving plant performance under drought stress. The phylogeny of aquaporins is well established based on model species like Arabidopsis thaliana, which can be used as a template to investigate aquaporins in other species. In this study we comprehensively identified aquaporin encoding genes in tomato (Solanum lycopersicum), which is an important vegetable crop and also serves as a model for fleshy fruit development. We found 47 aquaporin genes in the tomato genome and analyzed their structural features. Based on a phylogenetic analysis of the deduced amino acid sequences the aquaporin genes were assigned to five subfamilies (PIPs, TIPs, NIPs, SIPs and XIPs) and their substrate specificity was assessed on the basis of key amino acid residues. As ESTs were available for 32 genes, expression of these genes was analyzed in 13 different tissues and developmental stages of tomato. We detected tissue-specific and development-specific expression of tomato aquaporin genes, which is a first step towards revealing the contribution of aquaporins to water and solute transport in leaves and during fruit development.

/pdf/genome-wide-identification-and-expression-analysis-of-2uj34q53gz.pdf

Genome-Wide Identification and Expression Analysis of Aquaporins in Tomato

The mobility of sugars between source and sink tissues in plants depends on sugar transport proteins. Studying the corresponding genes allows the manipulation of the sink strength of developing fruits, thereby improving fruit quality for human consumption. Tomato (Solanum lycopersicum) is both a major horticultural crop and a model for the development of fleshy fruits. In this article we provide a comprehensive inventory of tomato sugar transporters, including the SUCROSE TRANSPORTER family, the SUGAR TRANSPORTER PROTEIN family, the SUGAR FACILITATOR PROTEIN family, the POLYOL/MONOSACCHARIDE TRANSPORTER family, the INOSITOL TRANSPORTER family, the PLASTIDIC GLUCOSE TRANSLOCATOR family, the TONOPLAST MONOSACCHARIDE TRANSPORTER family and the VACUOLAR GLUCOSE TRANSPORTER family. Expressed sequence tag (EST) sequencing and phylogenetic analyses established a nomenclature for all analyzed tomato sugar transporters. In total we identified 52 genes in tomato putatively encoding sugar transporters. The expression of 29 sugar transporter genes in vegetative tissues and during fruit development was analyzed. Several sugar transporter genes were expressed in a tissue- or developmental stage-specific manner. This information will be helpful to better understand source to sink movement of photoassimilates in tomato. Identification of fruit-specific sugar transporters might be a first step to find novel genes contributing to tomato fruit sugar accumulation.

Masahito Akiyama

Papers

Genome-Wide Identification and Expression Analysis of Aquaporins in Tomato

The sugar transporter inventory of tomato: genome-wide identification and expression analysis.