Aquaporins are channel proteins present in the plasma and intracellular membranes of plant cells, where they facilitate the transport of water and/or small neutral solutes (urea, boric acid, silicic acid) or gases (ammonia, carbon dioxide). Recent progress was made in understanding the molecular bases of aquaporin transport selectivity and gating. The present review examines how a wide range of selectivity profiles and regulation properties allows aquaporins to be integrated in numerous functions, throughout plant development, and during adaptations to variable living conditions. Although they play a central role in water relations of roots, leaves, seeds, and flowers, aquaporins have also been linked to plant mineral nutrition and carbon and nitrogen fixation.

Plant Aquaporins: Membrane Channels with Multiple Integrated Functions

https://www.researchgate.net/profile/Rupam_Kapoor/publication/26881549_Arbuscular_mycorrhizal_fungi_in_alleviation_of_salt_stress_A_review/links/0c960523fd2cc5ec7f000000.pdf

Arbuscular mycorrhizal fungi in alleviation of salt stress: a review.

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.

There is strong evidence that aquaporins are central components in plant water relations. Plant species possess more aquaporin genes than species from other kingdoms. According to sequence similarities, four major groups have been identified, which can be further divided into subgroups that may correspond to localization and transport selectivity. They may be involved in compatible solute distribution, gas-transfer (CO2, NH3) as well as in micronutrient uptake (boric acid). Recent advances in determining the structure of some aquaporins gives further details on the mechanism of selectivity. Gating behaviour of aquaporins is poorly understood but evidence is mounting that phosphorylation, pH, pCa and osmotic gradients can affect water channel activity. Aquaporins are enriched in zones of fast cell division and expansion, or in areas where water flow or solute flux density would be expected to be high. This includes biotrophic interfaces between plants and parasites, between plants and symbiotic bacteria or fungi, and between germinating pollen and stigma. On a cellular level aquaporin clusters have been identified in some membranes. There is also a possibility that aquaporins in the endoplasmic reticulum may function in symplasmic transport if water can flow from cell to cell via the desmotubules in plasmodesmata. Functional characterization of aquaporins in the native membrane has raised doubt about the conclusiveness of expression patterns alone and need to be conducted in parallel. The challenge will be to elucidate gating on a molecular level and cellular level and to tie those findings into plant water relations on a macroscopic scale where various flow pathways need to be considered.

Plant aquaporins: multifunctional water and solute channels with expanding roles.

It is clear that stomata play a critical role in regulating water loss from terrestrial vegetation. What is not clear is how this regulation is achieved. Stomata appear to respond to perturbations of many aspects of the soil-plant-atmosphere hydraulic continuum, but there is little agreement regarding the mechanism (or mechanisms) by which stomata sense such perturbations. This review discusses feedback and feedforward mechanisms by which hydraulic perturbations are putatively transduced into stomatal movements, in relation to generic empirical features of those responses. It is argued that a metabolically mediated feedback response of stomatal guard cells to the water status in their immediate vicinity ('hydro-active local feedback') remains the best explanation for many well-known features of hydraulically related stomatal behaviour, such as transient 'wrong-way' responses and the equivalence of hydraulic supply and demand as stomatal effectors. Furthermore, many curious phenomena that appear inconsistent with feedback, such as 'apparent feedforward' humidity responses and 'isohydric' behaviour (water potential homeostasis), are in fact expected to emerge from the juxtaposition of hydro-active local feedback and the well-known hysteretic and threshold-like effect of water potential on xylem hydraulic resistance.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.2005.01543.x

The control of stomata by water balance.

The prime function of aquaporins (AQPs) is generally believed to be that of increasing water flow rates across membranes by raising their osmotic or hydraulic permeability. In addition, this applies to other small solutes of physiological importance. Notable applications of this 'simple permeability hypothesis' (SPH) have been epithelial fluid transport in animals, water exchanges associated with transpiration, growth and stress in plants, and osmoregulation in microbes. We first analyze the need for such increased permeabilities and conclude that in a range of situations at the cellular, subcellular and tissue levels the SPH cannot satisfactorily account for the presence of AQPs. The analysis includes an examination of the effects of the genetic elimination or reduction of AQPs (knockouts, antisense transgenics and null mutants). These either have no effect, or a partial effect that is difficult to explain, and we argue that they do not support the hypothesis beyond showing that AQPs are involved in the process under examination. We assume that since AQPs are ubiquitous, they must have an important function and suggest that this is the detection of osmotic and turgor pressure gradients. A mechanistic model is proposed--in terms of monomer structure and changes in the tetrameric configuration of AQPs in the membrane--for how AQPs might function as sensors. Sensors then signal within the cell to control diverse processes, probably as part of feedback loops. Finally, we examine how AQPs as sensors may serve animal, plant and microbial cells and show that this sensor hypothesis can provide an explanation of many basic processes in which AQPs are already implicated. Aquaporins are molecules in search of a function; osmotic and turgor sensors are functions in search of a molecule.

What are aquaporins for

When perfused with a saline medium whose tonicity ranged from 400 mosmolar down to near 1 mosmolar Necturus gall bladder transferred volumes of fluid which were quasi-isotonic. At the very low pressures pertaining during an experiment, the flow rates could not be explained by simple mechanical filtration and were inhibited by pretreatment with ouabain, indicating that the fluid transfer was an active secretion by the epithelial cells. Electron micrographs of the cells show that at the lower osmolarities used the epithelial cells were swollen but intact. Dimensions of the lateral interspaces obtained from both transmission and scanning electron micrographs have been used to calculate the osmolarity of the secretion as a function of bathing osmolarity, according to standing-gradient osmotic theory. The results show that the theory cannot possibly provide an acceptable description of the fluid production, and that the water is almost certainly crossing the epithelium by an extracellular route through the intercellular junctions.

Fluid Transfer by Necturus Gall Bladder Epithelium as a Function of Osmolarity

Pollen tube growth is central to the sexual reproduction of plants and is a longstanding model for cellular tip growth. For rapid tip growth, cell wall deposition and hardening must balance the rate of osmotic water uptake, and this involves the control of turgor pressure. Pressure contributes directly to both the driving force for water entry and tip expansion causing thinning of wall material. Understanding tip growth requires an analysis of the coordination of these processes and their regulation. Here we develop a quantitative physiological model which includes water entry by osmosis, the incorporation of cell wall material and the spreading of that material as a film at the tip. Parameters of the model have been determined from the literature and from measurements, by light, confocal and electron microscopy, together with results from experiments made on dye entry and plasmolysis in Lilium longiflorum. The model yields values of variables such as osmotic and turgor pressure, growth rates and wall thickness. The model and its predictive capacity were tested by comparing programmed simulations with experimental observations following perturbations of the growth medium. The model explains the role of turgor pressure and its observed constancy during oscillations; the stability of wall thickness under different conditions, without which the cell would burst; and some surprising properties such as the need for restricting osmotic permeability to a constant area near the tip, which was experimentally confirmed. To achieve both constancy of pressure and wall thickness under the range of conditions observed in steady-state growth the model reveals the need for a sensor that detects the driving potential for water entry and controls the deposition rate of wall material at the tip.

/pdf/an-osmotic-model-of-the-growing-pollen-tube-1o6h1kd53j.pdf

An Osmotic Model of the Growing Pollen Tube

Experiments were performed with the perfused rat submandibular gland in vitro to investigate the nature of the coupling between transported salt and water by varying the osmolarity of the source bath and observing the changes in secretory volume flow. Glands were submitted to hypertonic step changes by changing the saline perfusate to one containing different levels of sucrose. The flow rate responded by falling to a lower value, establishing a new steady-state flow. The rate changes did not correspond to those expected from a system in which fluid production is due to simple osmotic equilibration, but were much larger. The changes were fitted to a model in which fluid production is largely paracellular, the rate of which is controlled by an osmosensor system in the basal membrane. The same experiments were done with glands from rats that had been bred to have very low levels of AQP5 (the principal aquaporin of the salivary acinar cell) in which little AQP5 is expressed at the basal membrane. In these rats, salivary secretion rates after hypertonic challenges were small and best modelled by simple osmotic equilibration. In rats which had intermediate AQP5 levels the changes in flow rate were similar to those of normal rats although their AQP5 levels were reduced.

AQP and the Control of Fluid Transport in a Salivary Gland

The evidence that a major fraction of water crosses the paracellular route during isotonic fluid transfer is reviewed together with a description of the theory and experimental results derived from extracellular probe studies Four transporting epithelia which have been studied using the method are gallbladder, intestine, Malpighian tubule, and salivary gland It is concluded that paracellular probe flows are not due to simple convection generated by osmotic flow through the junctions but are generated by active fluid transport within the junction: a mechano-osmotic process The geometry of the pathway involved would indicate that some salt accompanies the paracellular fluid, representing a hypo-osmotic flow Transport of salt by the cell route, which may be accompanied by some water, represents a hypertonic flow The problem then becomes one of balancing the two to produce an isotonic transportate We suggest, using recent data from knockout mice, that some aquaporins are functioning in different epithelial tissues as osmo-comparators within a feedback loop that regulates the paracellular fluid flow rate This results in an overall quasi-isotonic transport by the epithelium The model is applied to forward-facing systems such as proximal tubule and backward-facing systems such as exocrine glands

A. E. Hill

Papers

What are aquaporins for

Fluid Transfer by Necturus Gall Bladder Epithelium as a Function of Osmolarity

An Osmotic Model of the Growing Pollen Tube

AQP and the Control of Fluid Transport in a Salivary Gland

Paracellular fluid transport by epithelia.