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Guttation: mechanism, momentum and modulation.

CONTENTS

Abstract

I.   Introduction
II.  Mode of Guttation
III. Mechanism of Guttation: Chain of Events
     1. Vital force theory of sap movement and exudation
     2. Physical force theory of sap movement and exudation
     3. Root pressure theory of sap movement and exudation: revisited
        as the main candidate for guttation
        a. Magnitude of root pressure
        b. Osmotic mechanism of root pressure
        c. Metabolic mechanism of root pressure
        d. Involvement of local pressure in the shoot and leaf for
           bleeding and guttation
     4. Integrated view of sap movement and guttation
        a. Root-mediated "pushing water up" hypothesis and guttation
        b. Compensating pressure theory and guttation
        c. Plant heart or water pump theory and guttation
        d. Chemico-mechanosensory signal and guttation
        e. Light signal and guttation
        f. Chemical signals travelling between opposite plant poles,
           i.e. shoot tips [??] root tips
        g. Molecular aspect of guttation : involvement of contractile
           proteins and aquaporins
        h. Energy coupling
        i. Gist of the mechanism at a glance
        j. The unknowns-where to go next?
IV.  Intensity of Guttation
V.   Regulation of Guttation
     1. Internal factors
        a. Species and genotypic variability
        b. Phenological variability
        c. Hormonal variability
        d. Enzymatic variability
     2. External factors
        a. Environmental factors
           i. Mechanical stimuli
           ii. Temperature
           iii. Light
           iv. Humidity
           v. Wind
        b. Edaphic factors
           i. Soil and root temperature
           ii. Soil moisture
           iii. Soil nutrients
           iv. Soil aeration
           v. Soil mycorrhizae
VI.  Conclusions and Future Perspectives
VII. Acknowledgements
     Literature Cited


Introduction

Guttation refers to the process of exudation of liquid droplets, i.e. loss of water from the tips, edges and adaxial and abaxial surfaces of uninjured leaves of a wide range of plant species (Singh & Singh, 2013; Singh, 2014a, b). It is one of several visible physiological phenomena known since last over three-and-a half centuries (Munting, 1672), providing a non-invasive identity of several chemical transformations and their mobility in plants. Though it is now known to play a significant role in the soil-plant-environment system (Singh, 2013) and in the production of a number of pharmaceutical products which were not earlier known (Komamytsky et al., 2000,2004,2006; Ma et al., 2003; Fischer & Schillberg, 2004), the mechanism underlying this phenomenon is not fully understood. However, lately the science of guttation has passed through several phases of change and advances wherein some important discoveries, both fundamental and applied, have been made in the fields relating to its structural biology (Sperry, 1983; Chen & Chen, 2005, 2006, 2007; Feild et al., 2005; Pillitteri et al., 2007, 2008; Wang et al., 2011), physiology (Ewers et al., 1997; Fisher et al., 1997; Enns et al., 1998; Pedersen, 1998; Quanzhi et al., 1999; Pilot et al., 2004; Aloni, 2001; Aloni et al., 2003, 2005; Aki et al., 2008; Singh et al., 2008, 2009a; Cao et al., 2012), biochemistry (Sze, 1984; Pedersen, 1993, 1994; Sze et al., 2002; Burkle et al., 2003; Pickard, 2003a, b; Wegner, 2014), plant microbiology and phytopathology (Ivanoff, 1963; French et al., 1993; Carlton et al., 1998; Gareis & Gareis, 2007) and biotechnology (Komamytsky et al., 2000, 2006; Rybicki, 2009). As form and function of cells and their components are intimately intertwined, they both go hand in hand in all living systems (Gasparikova et al., 2001; Baluska et al., 2006; Baluska & Mancuso, 2009, 2010). The hydathodes, in the present case, the microscopic machinery and mouths of guttation, absorb and retrieve solutes which are then secreted out of leaves (Goatley & Lewis, 1966; Ozaki & Tai, 1962; Lersten & Curtis, 1982, 1985; Gay & Tuzun, 2000; Pilot et al., 2004; Aki et al., 2008). Similarly, several signal transduction and transport proteins originating from both the shoot and root, are found in the guttation fluid that are also transported to the sites of active vegetative and reproductive growth where they are required for the formation and development of fruits and seeds in plants (Zholkevich, 1991; Pedersen, 1998; Scofield et al., 2007; Shepherd & Wagner, 2007; Slewinski et al., 2009,2010; Baskin et al., 2010). Therefore, in view of significance of guttation in transport of nutrients, water, proteins, enzymes, hormones and metabolites; maintenance of leaf and soil water status, and soil fertility; ecological balance and environmental sustainability; disease and insect pests resistance; enhancement of yield-sink potential; hydrostatic pressure release; non-invasive test for weedicides, fungicides, insecticides; and plant physiological investigations (Singh, 2013) and production of pharmaceuticals for human use (Komamytsky et al., 2000,2004,2006; Ma et al, 2005); unlocking and understanding the mystery of guttation is imperative. In this review paper, I have attempted to highlight the new and latest findings and discoveries that throw light on the plausible integrated view of the mechanism of guttation and its regulation.

Mode of Guttation

The mode of guttation constitutes the sequence of events of sap movement supposedly originating in roots passing en route through the stem and possibly controlled and regulated in the leaves as well before culminating into exudation from hydathodes in liquid form as guttation. What exactly triggers its origin and subsequent translation into the initiation and final exudation at the end point in leaves is not known, despite the occurrence of this phenomenon in a wide range of plants when conditions favor rapid absorption of water and low transpiration (Barrs, 1966; Klepper & Kaufmann, 1966; Zholkevich, 1991; Pedersen, 1993). For instance, when a well-watered, vigorously growing tomato plant is placed under a bell-jar, transpiration ceases as the atmosphere in the jar becomes saturated. Continued water absorption then results in a slow exudation of water from the tips of the leaves. Also, developed rice plants under conditions of still air with adequate soil moisture and high relative humidity profusely guttate in the field in situ both during day and night (Singh et al, 2008, 2009a). These exudations occur through epidermal and epithemal hydathodes (Haberlandt, 1914; Lepeschkin, 1923). In the former, water secretion is dependent on the metabolic activity of the specialized epidennal cells on the adaxial surface of leaves near vein endings, and this is regarded as an active process but occurs rarely. For epithemal hydathodes, on the other hand, the process is passive. They respond directly with the water-conducting system of the plant. The water passing out through hydathodes as droplets can be observed when "root pressure" reaches a certain threshold, as a result of an inhibited or reduced transpiration (Canny, 1995; Kundt, 1998; Pickard, 2003a, b; Kundt & Gruber, 2006; Wegner, 2014; Singh, 2016).

At night or before sunset, transpiration usually does not occur because most plants have their stoma closed which is followed by guttation. Guttation is found to occur in plants mostly in well irrigated land. When there is a high soil moisture level, water will enter plant roots, because the water potential of the roots is lower than the soil solution. Thus, water will accumulate in the roots creating a hydrostatic pressure. The root pressure forces some water to exude through hydathodes located at the tips, edges, adaxial and abaxial surfaces of leaves forming drops of guttation. The root pressure, essentially a phenomenon of "pushed up" rather than "pulled up" process provides the impetus for the evolution of the exudation force and its flow. It is generally agreed that the process of guttation takes place due to root pressure (Singh & Singh, 1989; Fisher et al., 1997; Pedersen & Sand-Jensen, 1997; Dustmamatov et al., 2004; Singh et al., 2009b) whose mechanism is not fully understood however, very recently a new headway has been made to the understanding of this phenomenon (Wegner, 2014).

Mechanism of Guttation: Chain of Events

From time to time, many theories have been put forward by various workers to explain the mechanism of upward movement of sap, a primary and necessary requirement for guttation to occur as the sap has to travel to tips and edges of leaves for its exudation as droplets. These theories and postulates constitute either the part of vital force theory or physical force theory or root pressure theory or the combination of all of these theories not fully and precisely known todate.

1. Vital force theory of sap movement and exudation

Vital theories presume that the ascent of sap resulting in exudation of fluid is due to the vital activity of living cells of the plants. In this regard Godlewski (1884) proposed "relay pump theory" and Bose (1923) propounded "propulsive pulsation theory" of ascent of sap (Singh, 2009; Shepherd, 2012). It would seem that, under conditions of active root growth and with an ample supply of reserve foods, the root cells are, as a result of vital activity, capable of absorbing water against pressure. Vigorously growing vines in spring may exhibit guttation as manifestation or expression of pressurized sap. In this context, the propulsive pulsation theory of Bose (1923), a physicist-turned-plant physiologist and known as the father of Indian plant physiology, is of particular interest. He assumed that the pulsatory activity like heart beat is found in the inner cortical cells which are situated in the vicinity of the endodennis. As a result of this pulsatory activity which is automatic in nature, water is forced or pumped into cavities (vessel) of xylem and water moves upward (Shepherd, 2012). However, the views of vital theories were discarded, though erroneously, on the ground that the living cells are not essential for ascent of sap, as when the living cells were killed (destroyed) by picric acid or HgCl2 solution, the ascent of sap continued. But in view of relatively recent discovery of contractile proteins (Abutalybov & Zholkevich, 1979; Abutalybov et al, 1980; Baluska & Volkmann, 2008) and aquaporins (Steudle, 2001; Maurel et al, 2008; Kaldenhoff et al, 2008, 2014), and also recently the findings on the effects of roots and leaves excision, pneumatic pressure application to the excised stem, use of metabolic inhibitors on the ascent of sap (Singh et al, 2009b) have raised points for the revival of debate on Bose's pulsation theory. The author of this review, like others (Eaton, 1943; Lundegardh, 1944), is of the view that the vital forces or activities seem to be involved in the process of development of root pressure in one way or the other hence causing the ascent of sap culminating into guttation in plants whether they are apparently visible or invisible (Kundt, 1998; Pickard, 2003a, b; Kundt & Gruber, 2006; Wegner, 2014; Singh, 2016).

2. Physical force theory of sap movement and exudation

According to this theory, various physical principles such as electro-osmosis, capillary action, imbibitional forces, atmospheric pressure etc. (Nobel, 2005) have been suggested as the driving force for the ascent of sap leading to guttation. However, the involvements of these physical forces for the upward movement of sap in plants have not been experimentally proved without controversies. Lundegardh (1944), for example, was unable to find a potential difference of more than 100 millivolts between the surface and the interior of wheat roots. In contrast, his calculations indicated that a potential gap of 150,000 millivolts would be required to raise water to a height of 100 cm in tubes 0.63 [micro]m in diameter. The vessels in wheat roots are much wider than this. Consequently, it appears that electro-osmotic forces are of insufficient magnitude to play a significant role in the maintenance of pressure differences of water across plant membranes or plant height. However, early physiologists (Flood, 1919; Priestley, 1920; White, 1938; Tazaki, 1939) were familiar with the bleeding and guttation and ideas were advanced that pressures developed in the xylem because of a uni-directional inward secretion of water were responsible for fluid exudation. Attempts were also made to account for the polar movement of water on a basis of differences in permeability however, none of these ideas was successful in explaining the phenomenon to the extent required for guttation or bleeding in plants.

3. Root pressure theory of sap movement and exudation', revisited as the main candidate for guttation

Historically, the term "root pressure" was first coined by Hales (1727) who, in the first published account of the phenomenon, described bleeding and bleeding pressures developed by a grapevine that had been pruned heavily. However, while characterizing guttation, its flow is to be viewed in an integrated manner with those of the absorption of water, hydrostatic pressure and upward translocation by bunching them together, rather considering them separately and individually (Fig. 1). Very recently, a comprehensive account of the mechanism of root pressure, its regulation and significance in plants has been published by the author of this review article (Singh, 2016) and the interested scholars are advised to consult this publication to have a firsthand elaborate information on this phenomenon. Guttation is primarily considered as the manifestation and expression of root pressure which is also known as "exudation pressure". It is generally agreed that roots generate positive hydrostatic pressure by absorbing ions from the dilute soil solution and concentrating them into the xylem (Stocking, 1956a; Zholkevich, 1991; Pedersen, 1993, 1994). The buildup of solutes in the xylem sap leads to a negative osmotic potential and thus a decrease in the xylem water potential. This lowering of the xylem water potential provides a driving force for water absorption, which in turn, leads to a positive hydrostatic pressure in the xylem (Kramer & Currier, 1950; Boyer, 1985). It is thus, the root pressure which provides motive and driving force that is responsible for pushing the water up and finally out of permanently open hydathodes resisting the pull of gravity (Crafts and Broyer, 1938; White, 1938; Arnold, 1952; Stocking, 1956b; Zholkevich, 1991; Pickard, 2003a, b; Dustmamatov et al., 2004; Taiz & Zeiger, 2006). It is possible that root pressure reflects an unavoidable consequence of high rates of ion accumulation (Palmgren, 2001; Gaxiola et al., 2007; Morth et al., 2011). However, the existence of positive pressures within the xylem at night can help dissolve previously formed gas bubbles, and thus play an evolutionary and ecological role in reversing the deleterious effects of cavitation and embolism under stressful situations (Holbrook et al., 2001; Brodribb & Holbrook, 2006; Singh et al., 2009b).

Root pressures in temperate climate most frequently develop during warm nights though most of water transport occurs during day time. Significant and consistent root pressures are developed in a wide range of plant species (Fisher et al., 1997; Zholkevich, 1991; Ewers et al., 1997). Moreover, root pressure develops not only in the herbaceous species but in deciduous trees such pressures are demonstrable in the spring before the buds open, but once the leaves have expanded and rapid water movement through the plant begins, root pressure can no longer be detected but continues to exist invisibly (Feild et al., 2005; Feild & Arens, 2007). These pressures keep on fluctuating generally within a range of 50 to 300 kPa varying with species, growing conditions, environmental, and edaphic factors etc. accompanied by seasonal and diurnal periodicity.

a. Magnitude of root pressure

White (1938) recorded pressures of 600 to 700 kPa in excised tomato roots. A pressure of 700 kPa, though capable of causing a flow of water in the xylem of tall trees, but in view of existence of resistance to flow, cavitation etc. may not be sufficient to push the water in most of the tallest trees. However, Davis (1961) suggested that force causing the flow of sap was very high which exists in the living cells of the roots. Such magnitudes of root pressure would certainly be no problem for either agricultural field crops (Singh & Singh, 1989; Tanner & Beevers, 1999, 2001; Singh et al, 2009b) or palm trees (Davis, 1961) or deciduous forest trees (Feild et al, 2005; Feild & Arens, 2007; Cao et al., 2012) acting as supplementary device to cohesion-tension mechanism (Steudle, 2001) for upward movement of sap in rapidly transpiring plants.

b. Osmotic mechanism of root pressure

In fact, a series of observations contradict the simplified schemes and reveal the complicated nature of root pressure, which is summarized by two principally different constituents. Conditionally, these constituents can be respectively referred to as osmotic and metabolic in nature. According to the osmotic concept, the root pumping activity equates to the osmometer work and the driving force for exudation is determined by the difference in osmotic potential (OP) between the xylem sap and the ambient solution enabling the exudation impossible in hypertonic solutions (Priestley, 1920). Thus, the net flow of water across a semi-permeable membrane will typically be from a higher to lower water potential. In the absence of a semi-permeable barrier, the movement of water and dissolved solutes occurs along gradients in pressure (i.e. from regions of higher pressure to lower one). This leads to the development of root pressure, i.e. a positive hydrostatic pressure in the tracheary elements of the xylem resulting in fluid exudation in the fonn of droplets either from cut stumps or tips and margins of uninjured leaves. However, the osmotic pressure of the ambient solution at which exudation stops, considerably exceeds the osmotic pressure of the exudates contradicting the osmotic concept of root pressure. Therefore, a number of authors (Broyer, 1951; Ginsburg & Ginzburg, 1971; Zholkevich, 1991) came to the conclusion that a metabolic component (non-osmotic) of root pressure must exist. Additionally, the water potential of the guttation fluid is usually higher than that of the ambient solution (Oertli, 1966, 1986; Wegner, 2014). The above-mentioned facts therefore, contradict the osmotic concept, which equates the root pumping activity to the osmometer work. Such facts demonstrate the complicated nature of root pressure and indicate that the living cells of xylem parenchyma take an active part in root pressure build-up. To a certain degree, their function resembles secretion; it depends on metabolic energy supply, cell polarization, cell membrane intactness, contractory and sensory systems such as actin and myosin and probably, mediator regulation (Zholkevich, 1991; Staiger et al., 2000; Pickard, 2003a, b; Baluska et al., 2006; Baluska, 2010). Obviously, the dictate and direction of water flow by xylem parenchyma cells need further investigations for the elucidation of the mechanism of root pressure (Wegner, 2014; Singh, 2016).

c. Metabolic mechanism of root pressure

Russian workers headed by Zholkevich in Moscow consider sleeves (root segment without stele, i.e. stele surgically removed) especially suitable for studying water transport via roots because they have no stele, with its hypothetical apoplasm channels (Zholkevich et al., 1989; Dustmamatov et al., 2004). Some authors tried to explain the root pressure mechanism by the functioning of these channels (Katou et al., 1987). The sleeve exudation occurs only at the expense of the metabolic component. As to the osmotic component, at first it is absent. The osmotic component begins gradually to participate in the transport processes as the exudate fills the hollow of the removed stele. Observations made on the sleeve exudation rate with the roots of 5-day-old Zea mays seedlings proved to be twice as high as that of the whole root (Zholkevich et al., 1989). The value of [Q.sub.10] of the sleeve exudation was close to 5, whereas that of the whole-root exudation rate was close to 3. Thus, the metabolic processes appear to play a greater role in the sleeve exudation than in that of the whole root, they claimed (Tarakanova et al., 1985; Tarakanova & Zholkevich, 1986). If the water transport mechanism is associated with a metabolic component and with the participation of living cells, it seems that the water moves via these cells and not only via the apoplast (Korolev & Zholkevich, 1990). The fact that water moves mainly by symplastic and transvacuolar pathways was shown experimentally with a decapitated root system (Ginsburg & Ginzburg, 1970, 1971). How one should imagine the direct participation of xylem parenchyma cells in root pumping activity, is a matter to be looked into seriously however, very recently new and novel insights into this phenomenon have been advanced (Wegner, 2014). Further details of metabolic aspect of root pressure have been described in the next few pages as and when required.

d. Involvement of local pressure in the shoot and leaf for bleeding and guttation

Some of the best known examples of the bleeding of sap from cuts and wounds in trees are not a result of pressures developed through root activity but rather are brought about by local conditions within the stems or branches themselves. The copious flow of sap from cuts and bore holes in the sugar maple (Acer saccharum) that occurs under conditions in which few other plants show bleeding is a familiar example of this phenomenon. As much as 150 1 of sap have been obtained from a single vigorous tree, although the average yield is from 25 to 75 1 of sap in a season. The bleeding phenomenon of sugar maple is associated with the storage of large quantities of starch, sucrose and hexose in the xylem during the summer. As a result of hydrolysis of the starch to sugar in the winter before sap flow begins, a high concentration of osmotically active material is found in wood. Johnson (1945) found that about five times as much sap was obtained from the stump of a tree cut two feet above ground level as from the same cut tree when it was suspended by attaching it in an upright position to another tree. A further example of bleeding that results from locally developed stem pressures is the exudation obtained from several types of palms. Sap quantities as much as 10 1a day from Phoenix dactylifera and more than 1000 1 during the entire season from a single Indian date palm (Phoenix sylvestris) have been noted (Bose, 1923). Of further interest, a single tree of Palmyra (Borassus flabellifera) may yield as much as 120,0001 of sap in its life time. Here again flow is stimulated by variously pounding, cutting, or otherwise injuring cells in which carbohydrates have accumulated. Thus, the exudation of sap is neither dependent on root pressure nor immediately dependent on a supply of water from roots but can result from a withdrawal of sap from the trunk. However, the relationship of these facts to the mechanism whereby flow is maintained is not yet clearly understood (Kramer, 1949). There is no reason to believe as to why such local pressures in the stem and epithem cells of hydathodes should not exist and cause guttation or exudation of fluid as Quanzhi et al., (1999) have recently noted higher-up bleeding in rice peduncle neck influencing panicle-sink quality.

4. Integrated view of sap movement and guttation

According to Fick's first law, the movement of molecules by diffusion always proceeds spontaneously, down a gradient of free energy or chemical potential, until equilibrium is reached (Fick, 1855). The spontaneous "downhill" movement of molecules is termed passive transport as the case of cohesion-tension (Dixon, 1914). At equilibrium no further net movements of solutes can occur without the application of a driving force. The movement of substances against or up a gradient of chemical potential is tenned active transport. It is not spontaneous, and it requires that work be done on the system by the application of cellular energy. One way (but not the only way) of accomplishing these tasks is to couple transport to the hydrolysis of ATP. The only situation in which water can be set to move across a semi-permeable membrane against its water potential gradient is when it is coupled to the movement of solutes (Wegner, 2014). The transport of sugars, amino acids and other small molecules by various membrane proteins can "drag" up to 260 water molecules across the membrane per molecule of solute transported (Loo et al., 1996). Such transport of water can occur even when the movement is against the usual water potential gradient (i.e., toward a larger water potential), because the loss of free energy by the solute is more than it compensates for the gain of free energy by the water. The net change in free energy remains negative. The amount of water transported in this way will generally be quite small compared to the passive movement of water down its water potential gradient. It is to be kept in mind that the biological transport can be driven by four major forces: gradient in concentration, hydrostatic pressure, gravity, and electrical fields. Proton transport is a major determinant of the membrane potential (Palmgren, 2001). The excess voltage is provided by the plasma membrane electrogenic [H.sup.+]-ATPase. The biological membranes contain transport proteins that facilitate the passage of selected ions and other polar molecules. The general term transport proteins encompasses three main categories of proteins viz, channels, carriers, and pumps. Transport proteins exhibit specificity for the solutes they transport, hence their diversity in cells. Channel proteins act as membrane pores, and their specificity is determined primarily by the biophysical properties of the channel. These channel transmembrane proteins function as selective pores, through which molecules or ions can diffuse across the membrane. Transport through channels is always passive, and because the specificity of transport depends on pore size and electric charge more than one selective binding, channel transport is only limited to ions or water (Fig. 1). Channels are not open all the time: channel proteins have structures called gates that open and close the pore in response to external signals like voltage changes, hormones, light and posttranslational modifications such as phosphorylation. For example, voltage-gated channels open or close in response to changes in the membrane potential (Pedersen et al., 2007). Carrier proteins bind the transported molecules on one side of the membrane and release it on the other side. Carrier proteins, unlike channels, do not have pores that extend completely across the membrane. In transport mediated by a carrier, the substance being transported is initially bound to a specific site on the carrier protein. Carriers are therefore, specialized in the transport of specific ions or organic metabolites. Binding causes a conformational change in the protein, which exposes the substance to the solution on the other side of the membrane. Transport is complete when the substance dissociates from the carrier's binding site. Primary active transport is carried out by pumps and uses energy directly, usually from ATP hydrolysis, to pump solutes against their gradient of electrochemical potential. The membrane proteins that carry out primary active transport of water molecules energetically uphill against the free energy of water are called pumps (Gaxiola et al., 2007; Wegner, 2014; Singh, 2016). Most pumps transport ions, such as [H.sup.+] or [Ca.sup.2+]. However, pumps belonging to the ATP-binding cassette (ABC) family of transporters can carry large molecules. In the plasma membranes of plants, fungi, and bacteria, as well as in plant tonoplasts and endomembranes, H is the principal ion that is electrogenically pumped across the membrane. The plasma membrane [H.sup.+]-ATPase generates the gradient of electrochemical potential of [H.sup.+] across the plasma membranes, while the vocuolar [H.sup.+]-ATPase and the [H.sup.+]pyrophosphatase ([H.sup.+]-PPase) electrogenically pump protons into the lumen of the vacuole and the Golgi cistemae. In plant plasma membranes, the most prominent pumps are those of [H.sup.+] or [Ca.sup.2+], and the direction of pumping is outward. Therefore, another mechanism is needed to drive the active uptake of mineral nutrients such as N[O.sub.3.sup.0] , S[O.sub.4.sup.2-], P[O.sub.4.sup.2-]; the uptake of amino acids, peptides, and sucrose (Bienert et al., 2011); and the export of [Na.sup.+], which at high concentrations is toxic to plant cells. The other important way that solutes can be actively transported across a membrane against their gradient of electrochemical potential is by coupling the uphill transport of one solute to the downhill transport of another. This type of carrier-mediated co-transport is termed secondary active transport, and it is driven indirectly by pumps. Active transport utilizes carrier-type proteins that are energized directly by ATP hydrolysis or indirectly as symporters and antiporters (Morth et al., 2011; Wegner, 2014; Singh, 2016). The transporter gene identification has aided greatly in the elucidation of the molecular properties of transporter proteins (Jasinski et al., 2003). The emerging picture of plant transporter genes shows that a family of genes, rather than an individual gene, exists in the plant genome for most transport functions. Within a gene family, variations in transport characteristics, mode of regulation, and in differential tissue expression give plants a remarkable plasticity to acclimate to a broad range of environmental conditions (Arango et al., 2003).

Like other enzymes, the plasma membrane [H.sup.+]-ATPase is regulated by the concentration of substrate (ATP), pH, temperature, and other factors. In addition, [H.sup.+]-ATPase molecules can be reversibly activated or deactivated by specific signals such as light, hormones, pathogen attack, and the like. The autoinhibitory effect of the C-terminal domain of [H.sup.+]-ATPase can also be regulated by protein kinases and phosphatases that add or remove phosphate groups to serine or threonine residues on this domain. Phosphorylation recruits ubiquitous enzyme-modulating proteins called 14-3-3 proteins, which bind to the phosphorylated region and are thought to thus displace the autoinhibitory domain, leading to [H.sup.+]-ATPase activation. However, the recent findings indicate that a phosphorylation in the C-terminal auto-inhibitory domain of the plant plasma membrane [H.sup.+]-ATPase activates the enzyme with no requirement for regulatory 14-3-3 proteins (Piette et al., 2011). Because plant cells increase their size primarily by taking up water into large, central vacuoles, the osmotic pressure of the vacuole must be maintained sufficiently high for water to enter from the cytoplasm. The tonoplast regulates the traffic of ions and metabolites between the cytosol and the vacuole, just as the plasma membrane regulates uptake into the cell. These functions are carried out by a new type of proton-pumping ATPase (vacuolar ATPase also called V-ATPase) and differs both structurally and functionally from the plasma membrane [H.sup.+]-ATPase (Isayenkov et al., 2010). The physiological role of all these enzymatic proteins in water transport and its culmination into guttation is a topic of great fundamental and applied significance which needs rigorous scrutiny and careful studies.

a. Root-mediated "pushing water up" hypothesis and guttation

In 1989, Singh and Singh by their simple experiments demonstrated that the upward movement of water in rice plant took place due to pressure essentially generated in the roots, not due to water potential gradients that exist between the top (shoot) and bottom (root) of the plant. Furthering their work, recently Singh et al. (2009b) have presented in their studies on rice, five distinct pieces of evidence of the existence of, at whole-plant level, a mechanism similar to that of a "water forced upward-like device". We concluded that at the whole-plant level, roots possessed enormous capacity to absorb perhaps through the involvement of some bio-regulator(s), aquaporins, and to propel water up to the shoot, depending on stronger or weaker physiological activity of roots (Passioura & Angus, 2010; Eshel & Beeckman, 2013). The potential role of the proposed mechanism of water transport that enables plants overcome the problem of ascent of water troubled by cavitation and embolism during freezing and/or intermittent dry spells every now and then facilitating survival of plants during such harsh climatic conditions and thus becoming supplementary stakeholder in the cohesion-tension mechanism, has been discussed for agronomic success of crops under stressful situations (Tyree, 2003; McDowell et al, 2008; Singh et al., 2009b).

b. Compensating pressure theory and guttation

Relatively recent work contradicting the assumptions of the tensions measured in the xylem sap in cohesion-tension theory (CT theory) by the pressure-chamber, was presented by Canny (1995). Under conditions causing significantly soil moisture stress leading to plant water stress, pressures down to -600 kPa have been found, but then cavitations occurred very readily. Measurements of the cavitation thresholds of water showed an average threshold of about -200 kPa. Thus, the uncertain foundations in the light of Canny's explanations of the cohesion theory were recalled even having been confirmed by Scholander's measurements with the pressure chamber of the existence of high tensions in the xylem (Scholander et al., 1965). Canny discovered that no high tensions, and no gradients of tension along the plant height existed but the operating pressure of the xylem is raised into a stable range by compensating tissue pressures (CTP) pressing upon the tracheary elements. The tissue pressure does not propel the transpiration stream, which is still driven by evaporation, but protects the stream from cavitation and evidence was presented for the existence of positive pressures in roots, wood, and leaves (Canny, 1995, 1997, 1998, 2001). Canny emphasized that the pressure-chamber measures the water potential, but this is the potential not of xylem in tension, but of the compensating pressure applied to the xylem. This new theory which was offered by Canny may explain the observations of Singh and his colleagues (Singh, 1986; Singh & Singh, 1989; Singh, 2004; Singh et al., 2009b) who presented concrete evidence for root-mediated "pushing water up" mechanism in plants leading to guttation.

c. Plant heart or water pump theory and guttation

It is important to mention that a renowned German astrophyscist Kundt (1998) and his colleague (Kundt & Gruber, 2006) have recently argued that all higher plants suck in water from the soil osmotically through the root hair zone and lift it up to heights of 140 m through the xylem and phloem vessels. According to them the endodermis jump which is realized by two layers of subcellular mechanical pumps in the endodermis walls are powered by an energy-rich compound ATP, or in addition by two analogous layers of such pumps in the exodermis. The so-established root pressure helps force the absorbed ground water upward, through the whole plant, and often out again, in the form of guttation, or exudation. These authors claimed that plants cannot do without water pumps, or hearts and concluded that the rise of ground water in plants, both low plants and high plants, is likely owed to these mechanical pumps in the root hair zone whose excess pressure helps propel the water columns in their xylem vessels. These observations lend support to those earlier described by Indian and Australian workers about ascent of sap in plants (Singh, 1986; Singh & Singh, 1989; Canny, 1995, 2001; Singh et al., 2009b) ultimately culminating into guttation.

d. Chemico-mechanosensory signal and guttation

Guttation, as stated earlier, is a physiological phenomenon in plants. It could be that like stomata the hydathodes play a vital role in sensing and driving environmental change in the initiation of guttation (Hetherington & Woodward, 2003; Pillitteri et al., 2008; Wang et al., 2011) as the ability to sense and respond to physical stimuli is of key importance to all living organisms (Baluska et al., 2003; Baluska & Mancuso, 2009; Ninkovic & Baluska, 2010). A number of these stimuli appear to be closely related and can be considered as chemico-mechanical stimuli produced by pH gradient, hormones; mechanical loading by snow, ice, fruit, wind, rainfall, touch, sound; turgor potential, membrane potential, temperature, light, touch, sound etc. influencing cellular contractile proteins and gating of aquaporins in the living cell. All organisms appear to perceive these chemico-mechanical signals, regardless of their taxonomic classification or life habit. The significant differences between taxonomic groups are found in the individual molecular components of the microstructure of the internal cellular sensing network and in the response of an individual organism to each chemico-mechanical stimulus (Baluska et al., 2003).

In this regard, recent advances have led to the proposal of a plant-specific chemico-mechanosensory network within plant cells that is similar to the previously described network in animal systems (Staiger et al., 2000; Baluska et al., 2003; Baluska & Mancuso, 2009). This sensory network is the basis for a unifying hypothesis which, as mentioned above, may account for the perception of numerous chemico-mechanical signals including pH gradient, hormones, gravitropic, thigmomorphic, thigmotropic, self-loading, growth strains, turgor pressure, xylem pressure potential, and sound (Telewski, 2006; Hayashi et al., 2006). Sensing changes in turgor appears cmcial to survival in plants as well. It is possible that changes in turgor impart mechanical stresses on the cytoskeleton-plasma membrane-cell wall (CPMCW) which serves as the chemico-mechanosensory network for plant cells. Sensing water potential within the plant via internal mechanical stresses at the cellular level brought about by plasmolysis and deplasmolysis of epithem cells of hydathodes following transpiration and guttation one after another inducing fluid-phase endocytosis in combination of root pressure which is always at work, could be the means for what is termed hydraulic signaling, providing a faster signaling and hydathodal response to changes in leaf water status leading to guttation than could be predicted by a root-generated chemical signal such as abscisic acid for exudation to occur. These aspects as important they are however, need to be studied in depth to unravel the mechanism of action of chemico-mechanosensory system for the initiation of guttation.

e. Light signal and guttation

The influence of light and darkness on guttation was studied by Engel and Friederichsen (1954) who reported on rhythms and periodicity in guttation under the impulse of light. The guttation of Zea mays coleoptiles increased when exposed to light with a maximum about two hours after start of illumination, and generally decreased during dark periods. This pattern was observed whether the light-dark periodicity was 12:12, 6:3, 3:3 or 2:2 h. In 1:1 h cycles however, other growth processes appeared to obscure this system. They also observed that the guttation reaction of oats to light and darkness was exactly opposite the com coleoptiles. These variations in responses to light suggest the possibility of existence of additional component for the transformations of stimuli into exudation of guttation. Taking this aspect a step further Szarek and Trebacz (1999) measured the membrane potential changes evoked by light in the presence of ion channel and proton pump inhibitors to elucidate the nature of the response and a possible link to guttation in gametophytes of the fem Asplenium trichomanes as well as Avena coleoptile which both exhibit guttation when illuminated (Mcintyre, 1994). A possible role of [Cl.sup.-] and [K.sup.+] fluxes in light-induced guttation was suggested linking the energy-dependency of the phenomenon (Pedersen, 1993, 1994) as well as oxidative gating of aquaporins by affecting permeability which, in turn, allows the passage of [K.sup.+]. and [Cl.sup.-] ions building osmotic pressure which forces guttation water out of hydathodes (Kim & Steudle, 2009). The effect of quality of light with respect to its precise mechanism of action on the exudation of guttation is not known, however.

f. Chemical signals travelling between opposite plant poles, i.e. shoot tips [??] root tips

In view of complicated nature of guttation, the interplay of phytohormones produced in the roots and shoots in long-distance signaling evidenced by variations in xylem sap cytokinin concentrations, shoot auxin level, auxin transport and auxin response seem to be operative for induction of natural guttation (Aloni, 2001; Aloni et al, 2005; Pillitteri et al., 2008). For instance, chemical signals, altered under and originating from roots, play an important role in the root-to-shoot communication in the movement of water from soil layers through roots and shoots to sustain plant growth. Further, one of the physiological functions of hydathodes lies in the retrieval of cytokinins from xylem sap in their epithem cells to prevent their loss during guttation. This is accomplished by the mediation of purine permeases (PUP) particularly AtPUP 1 and AtPUP2 in Arabidopsis (Burkle et al., 2003; Aki et al., 2008). The presence of cytokinins saved by purine permeases (PUP), entering partially or wholly in combination of other hormones such as ABA in the signaling system, might play crucial role in the initiation and control of guttation in the manner not yet fully understood. For example, expression of AtNCEDs, AtABA2, and AA03 genes in phloem companion cells and xylem parenchyma cells of turgid plants are probably the main site of ABA biosynthesis in unstressed plants and ABA and its precursors might be synthesized in vascular tissues and transported to target cells such as stomata, hydathodes and sites of root pressure and guttation (Koiwai et al., 2004). ABA by way of its presence in vascular bundles, roots, and leaves might influence gating of aquaporins resulting in increased permeability of water hence its increased transport pressing the water to exude as guttation. Light might also play the similar role through the involvement of this or the relative ratio of other hormones affecting the permeability of water and its exudation as guttation (Mcintyre, 1994).

g. Molecular aspect of guttation'. involvement of contractile proteins and aquaporins

On its way from the xylem of root and stem through the leaf to the stomata and hydathodes, water can either move through cell walls and intercellular spaces (apoplastic movement) or pass through cytosols crossing plasma membrane (symplastic movement) thus traveling from cell to cell through plasmadesmata to cross the different tissues. Although all these pathways are probably used to some degree but among these the living cells appear to contribute substantially to the overall leaf hydraulic conductance. In this context, the role of contractile proteins in water transport regulation deserves special attention (Staiger et al., 2000; Baluska & Volkmann, 2008; Zheng et al., 2009). The contractile actomyosin-and actin-like proteins functions are probably associated with self-oscillations of water transport, involving rhythmic micro-oscillations of the parenchyma cells pressure potential, i.e. their pulsations, or alternate opening and closing of special channels in the symplasm (Mozhaeva & Bulycheva, 1971; Mozhaeva & Pil'shchikova, 1972; Abutalybov & Zholkevich, 1979; Abutalybov et al., 1980; Dustmamatov et al., 2004). According to Bose (1923), the ascending water flow in plants is impossible without parenchyma cells pulsation which may involve electrical pulses implicating the role of such contractile proteins therein. It is necessary to have in mind a relative independence of water and ion transport. If water transport is really dependent on rhythmic cell contractions or reversible opening and closing of either plasmadesmata or of other special channels, the polarization of the cell and of entire symplasm should be an indispensable condition for unidirectional water flow; otherwise, the water will move in all directions. It is now becoming increasingly clear that the transcellular water flow is facilitated and regulated by water channels in the membranes, named aquaporins (AQPs). AQP expression and activity effectively regulate the leaf water balance in normal conditions and modify the cell membrane water permeability in response to different internal and external factors (Steudle, 2001; Maurel et al., 2008; Kim & Steudle, 2009). We now know that the permeability of aquaporins can be regulated in response to intracellular pH. Decreased rates of respiration can lead to increases in intracellular pH (Katsuhara et al., 2008). This increase in cytoplasmic pH alters the conductance of aquaporins involved in the movement of water across roots. The fact that aquaporins can be gated in response to pH and other signals such as osmolarity, turgor etc. provides a mechanism by which roots can actively alter their permeability to water in response to their local environment. Regulation also occurs at the level of gene expression. Aquaporins are highly expressed in epidermal and endodermal cells and in the xylem parenchyma which may be critical points for control of water movement. The role of AQPs therefore, appears to be a multifaceted phenomenon (Kaldenhoff et al., 2008, 2014; Katsuhara et al., 2008; Azad et al., 2009; Heinen et al., 2009) however, its involvement in the initiation of guttation as yet unknown, is a potential research opportunity to follow up in future. Interestingly, the activity of water channels is also affected by water- and salinity-stresses, solute concentration, temperature, heavy metals, oxidative stress, and by the deprivation of nutrients to the roots (Mahdieh et al., 2008). Water channel (aquaporin) activity in plasma membranes of roots is under metabolic control and is affected by many external parameters. It is not yet clear whether water channel activity is also affected by pressure gradients set up across the root cylinder in response to high net tensions [-transpiration pull (negative) + root pressure] in the xylem while transpiring vigorously.

h. Energy coupling

How does water transport work against pull of gravity? If a stem is cut off or decapitated, fluid oozes out from the cut stump. If roots are poisoned or deprived of ATP, it ceases. There is inconclusive proof of the active transport of water in such systems, but the question is not closed. In the absence of the pull of transpiration, and when it is low (at night, or during period of very high relative humidity), water is absorbed by osmosis following active absorption of ions. Energy supplied by the living cells is utilized in this process (Gaxiola et al., 2007; Morth et al., 2011). The above description of water intake unravels the role played by the cells of the roots. A process that is not fully understood, however, is the removal of water from the soil by the epidermal cells of the root and its movement into the xylem under sufficient pressure to produce "bleeding" or "guttation" (Kundt, 1998; Kundt & Gruber, 2006). Agreement has, however, not been reached that root pressure, bleeding and exudation of guttation fluid do in fact involve only osmotic forces and salt secretion. In order for exudation from cut stumps to occur, the root must be actively respiring. Oxygen and sugar are essential as certain respiratory inhibitors stop the process (Lundegardh, 1950) though, not completely by adding vanadate, perhaps because not all of the ATPases are inhibited (Sze, 1984; Pedersen & Sand-Jensen, 1997; Sze et al., 2002) or only part of the guttation phenomenon is directly dependent on energy conversion in the roots. However, clear-cut experiments separating effects of respiratory activity on salts and on water are yet to be devised.

The other factor which supports guttation being an energy-dependent process is temperature. Water uptake decreases when roots are subjected to low temperature or anaerobic conditions, or treated with respiratory inhibitors. Until recently, there was no explanation for the connection between root respiration and water uptake. At cell level, in order to create and maintain the concentration difference, active pumping of the solute is required. ATP will be needed for this maintenance. In most plant cells, the [H.sup.+]-ATPases are primary active transporter. The hydrogen-ion-gradient is used by cotransporters and exchangers. Active pumping leads to an increased solute concentration (Fig. 1). Because of this, there is a greater tendency for water to flow to the vascular bundle. At tissue level, the process of energy-coupling also takes place in the manner : pericycle [right arrow] ATP [right arrow] xylem. Water movement from the root to the leaf is largely, but not wholly, due to the evaporation-tension-cohesion mechanism in continuously transpiring plants and ATP is not needed for this process. However, in both the presence and absence of transpiration, ion transporters continue their function of ions pumping leading to water uptake and movement energetically uphill against the free energy gradient of water and transport unabated, as a consequence, resulting in build-up of root pressure and exudation of guttation (Wegner, 2014; Singh, 2016). Thus, it is relatively clear that the plant cell uses the energy produced in respiration and drives water absorption across plasmatic membrane as respiratory inhibitors [(dinitrophenol (DNP) and azide)] block water absorption and respiratory promoters (sugar) enhance water absorption. That is how metabolic absorption of water by plant cells takes place leading to development of root pressure culminating into guttation. Though the mechanism of guttation is not fully known, it is tentatively suggested to be programmed to proceed as per interdependent plant activities depicted in Fig. 1.

i. Gist of the mechanism at a glance

Taking root and shoot including leaves as a whole unit, the mode and mechanism of guttation fluid visible as droplets at the tips and along the margins of leaves has been briefly summarized hereunder. The overall process of guttation appears to be triggered in the presence of conditions favoring absolute reduction in and inhibition of transpiration (high humidity, still air, favorable air and soil temperature, abundant soil moisture) following perception of any of chemico-mechanosensors such as pH gradients and hormones (ABA, auxin, cytokinins) singly or in combination, temperature, light, turgor potential, membrane potential; influencing the contractile proteins and the gating of transporter proteins (plasma membrane and vacuolar ATPases) that give way to energy-driven influx of solutes, metabolites and water across membranes. At this juncture the involvement of hormones influences aquaporin's gating leading to enhanced permeability of water apart from its energetically uphill transport which gives rise to positive hydrostatic pressure translating into root pressure. The root pressure so-developed provides impetus to the upward flow of xylem sap intermingling on the way with phloem sap too. The saps reaching the tracheary endings then come under the influence of the sensing, chemically and/or environmentally, by hydathodes--permanently open pores providing least resistance to flow, enhance the liquid flow out in the form of droplets/drippings or sometime streams called guttation under overall intrinsic and extrinsic regulation of genetic, internal, external, and edaphic factors.

j. The unknowns--where to go next?

The observations on root pressure, guttation and bleeding may argue for a simple osmotic movement of water driven by metabolic energy, with the cell activities confined to the antecedent or concomitant movement of solutes. Yet, this is not the whole explanation. In any event, a simple explanation of the phenomenon in its entirety in terms of osmotic relations does not seem to be adequate and the root pressure, the rates of bleeding, exudation and guttation are indicative of the complexity of causes and effects involved in these processes. It would be very interesting to thoroughly investigate the structural biology of hydathodes including their initiation and differentiation and root hairs and the regulation of root pressure using functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) techniques to gauge how various signals originating from and reaching to these tissues finally interact to initiate guttation as imaging may show activities milli--or micro--or even nano-seconds after it is activated to begin (Holbrook et al., 2001; Van As, 2007). In addition, new frontiers in guttation research also appear to be heading following the work of Komamytsky et al. (2000, 2004, 2006) who using genetic tricks with tobacco (Nicotiana tabacum L. cv Wisconsin) plants engineered to secrete human placental alkaline phosphatase (SEAP), green fluorescent protein (GFP) from jellyfish (Aequorea victoria), and xylanase from Clostridium thermocellum through the plant cell default secretion pathway. Further work might enable a better understanding not only of the structural biology of guttation but also help us leam about the function and mechanism of guttation as to when and how the switch of guttation is turned "on" and left "on" and switched "off".

Intensity of Guttation

The amount of guttation fluid depends upon its intensity and duration and the magnitude of root pressure which, in turn, are governed and regulated by several plant, environmental and edaphic factors (Fisher et al., 1997). The root pressure required to drive a mass flow of water also depends on whether or not an ion-concentrating mechanism is invoked. For a 1 m Myriophyllum plant the minimum root pressures required are 5 and 715 kPa, respectively (Pedersen, 1994). The important point to note is that efficiency of transport strongly depends on the dimensions of the xylem vessels (to the 4th power), the length of the plant, and the nutrient concentration of the root medium. It may be summarized that pressures of 100 to 200 kPa are commonly recorded when manometers are attached to decapitated plants but higher ones have occasionally been observed. The most generally accepted explanation of these root pressures is based on active accumulation of solutes by root cells, their secretion into the xylem, and the subsequent osmotic movement of water along the diffusion pressure gradient thus established (Bai et al., 2007; Zhu et al., 2010). Thus, the volume of guttated liquid is exceedingly variable. Only a few drops of water are commonly forced out at the tips and along the margins of leaves. The average total volume of guttation water exudate per grass blade per night was 1.0 [+ or -] 0.3 x [10.sup.-7] [dm.sup.3], which represents the comparable amount of water as dewfall to a short grass surface (Hughes & Brimblecombe, 1994). It was possible to collect from 1 to 3 mL of guttation solution from tomato plants at one time and to repeat the collection after a few hours (Raleigh, 1946). The volume of guttation fluid collected from the 2-month-old transgenic tobacco plants was 1 to 2 mL/g of leaf dry weight per day (up to 5 mL/[cm.sup.2] of leaf area) which contained up to 20 mg/mL (40 mg/g of leaf dry weight per day) of total soluble protein (Komamytsky et al, 2000). Guttation fluid production from bean leaves was recorded at the level of 6 mL/[cm.sup.2] of leaf area (Yarwood, 1952), whereas guttation fluid of rice (Oryza sativa) contained 25 mg/mL of copper-Folin-positive substances (Ozaki & Tai, 1962). Guttation from barley can vary with the age and the composition of the culture solution (Dieffenbach et al., 1980a, b) and the best rates of guttation were obtained with the primary leaves of 6- to 7-day-old seedlings grown on full mineral nutrient solution. However, modern varieties of rice have been noted to guttate very profusely, some of them exuded 271 [micro]L/tip/h, in addition to guttating from margins, adaxial and abaxial surfaces of the leaves as well during the day and through the night hours under field conditions in situ (Singh et al., 2008, 2009a). Some tropical plants too are stated to guttate so vigorously on humid nights that water literally drips from them (Feild et al., 2003, 2005). In fact, single leaves of Colocasia antiquorum are known to guttate upto 100-250 mL of water per night (Flood, 1919; Dixon & Dixon, 1931; Tazaki, 1939; Stocking, 1956b). The polypores of fungus Polyporus squamosus which is parasitic and saprobic found on living or dead trunks of deciduous trees or stumps and logs, exude droplets of water profusely and apparently seems like "dewatering" indicating an intensive guttation exudation similar to that in higher plants (Emberger, 2008).

Further, some plants can contribute more water through natural guttation to the soil than they lose through evaporation. This is called "cloud stripping" and is important source of water for creeks in some areas. Often, when the plants are cleared the creeks dry up. In tropical rain forests, where it is warm and humid all the time, guttation fluid drips from shrubs and small trees, mimicking rain. Making a departure from the usual observation on guttation in terrestrial plants, Pedersen (1993) measured the guttation in submerged aquatic plants S. emersum and L. dortmanna which showed the highest rates in young leaves. Guttation rates were 10-fold higher in the youngest leaf of S. emersum (2.1 [micro]L [leaf.sup.-1] [h.sup.-1]) compared with the youngest leaf of L. dortmanna (0.2 [micro]L [leaf.sup.-1] [h.sup.-1]). Singh et al. (2009a) discovered significant genotypic variability in the ability of guttation ranging from 62 to 110 [micro]L during half-an-hour period, with cultivars NDRH-2 registering the highest and Mahsuri the lowest values, respectively which were positively correlated with their panicle-sink potentials. Though it is difficult to a certain extent to compare the volumes being in different units of guttation fluid exuded by different species of plants, they do indicate a wide range of variability in the capacity to guttate at the species and genotypic levels whose mystery and significance are unclear and have not been resolved.

Regulation of Guttation

There are a number of factors that regulate the phenomenon of guttation. These factors may conveniently be classified into internal factors such as variabilities at species, genotypes, growth phenology, hormone physiology, enzyme levels etc. and external factors such as mechanical stimuli, temperature, light, humidity, wind velocity etc. and edaphic factors such as temperature, moisture, nutrients, aeration, mycorrhizae etc. of soils.

1. Internal factors

a. Species and genotypic variability

The phenomenon of guttation, though genetically governed, is greatly influenced by several environmental and edaphic factors. Evidently, it occurs in a wide range of plant species which include herbaceous mesophytes, shrubs and woody trees in angiosperms; gymnosperms and pteridophytes in addition to algae and fungi (Singh, 2014b). There is however, lack of information on genotypic differences in guttation among field and horticultural crops, though the rate of guttation differs widely among varieties thereof too. Bugbee and Koemer (2002) reported, USU-Apogee wheat cultivar having significantly high rates of guttation during dark periods and guttation occurred even during the light period when the stomates were partly closed by elevated C[O.sub.2]. Similar varietal and species responses to guttation phenomenon were observed among Satsuma oranges, and between Satsuma and grape fruit varieties, the later showed only occasionally traces of salt deposited by guttation (Long et al., 1956). Fujii and Tanaka (1957) examined the difference in the guttation and bleeding of seedlings of various varieties of rice. The guttation increased in parallel with the lateness of varieties, i.e. latematuring varieties exuded always greater amount of fluid than those of early-maturing ones which related to their root activities. Recently, Singh et al. (2008, 2009a) also found large genotypic variability in guttation rate among modern rice cultivars which is correlated with their panicle-sink potentials. The reasons for varietal differences in guttation are not fully known but could be attributed to difference in distribution of hydathodes, vessel dimensions, number of vessels, flow velocity, pressure gradient, root pressure, hydraulic resistance or its conductance (Pedersen, 1993). Variation in the composition and concentration of hormones and enzymes could possibly also be the reason to account for varietal differences in guttation which need thorough investigations with a view to understanding their link to nutrient-use, water-use and regulation of sink potential for enhanced productivity.

b. Phenological variability

Phenological variability, i.e. effect of growth stage, leaf location, leaf length and leaf age on guttation has also been studied (Pedersen, 1993, 1994). Ogura (1958) noted that up to third leaf stage the rate of guttation of upland rice seedlings was inferior to those of lowland rice seedlings however, reverse was true after the fourth leaf stage. The observations recorded on guttation from leaf tips at tillering, heading, anthesis, milk, dough and maturity stages in rice indicated that the cumulative volumes of exuded fluids per leaf tip during half-an-hour period were maximal at anthesis (132 [micro]L) followed by those at tillering (120 [micro]L), heading and milk stages being almost equal (112 [micro]L) and dough stage (42 [micro]L) (Singh, 2004; Singh et al., 2009a). At maturity no guttational oozing was observed from rice leaves. Guttation from the leaves of barley seedlings depends on age and on the composition of culture solution (Dieffenbach et al., 1980a). Also, occlusion of the hydathodes in older strawberry leaves has been reported (Bald, 1952; Takeda et al., 1991). Removal of waxes blocking the hydathodes in nonguttating strawberry leaves initiated guttation, suggesting that the main resistance to water flow was the wax deposit and other substances excreted through the hydathodes. Thus, an age-dependent occlusion of the hydathodes may result in this uneven pattern of guttation rates observed between leaves of different ages. Intensive studies are however, required to establish the ecological and agricultural significance of phenological variabilities in guttation.

c. Hormonal variability

The presence of a number of plant hormones in xylem and phloem saps which find their way in the guttation fluid has been recently described (Fletcher & Mader, 2007; Thompson et al., 2007). Along these lines, the addition of abscisic acid (ABA) at [10.sup.-6] to [10.sup.-4] M to the root medium was found to increase volume flow of guttation and exudation and the amount of [K.sup.+] exported 0-2 h after addition (Dieffenbach et al., 1980b). There was an ABA-dependent increase in water permeability (Lp) of exuding roots shortly after ABA addition. Later Lp was decreased by 35 % and salt export by 60 % suggesting an effect of ABA on salt transport to the xylem apart from its effect on Lp. Benzyladenine (5 x [10.sup.-8] to [10.sup.-5] M) and kinetin (5 x [10.sup.-6] M) progressively reduced volume flow and [K.sup.+] export in guttation and exudation and reduced Lp. Further, treatment of cucumber seedlings with 100 pL [L.sup.-1] of ethylene for 16 h increased the peroxidase activity of stem exudates and inhibited the amount of exudate released (Biles & Abeles, 1991). These observations suggest that xylem sap peroxidase may play a role in plugging damaged vascular tissue affecting thereby the phenomenon of guttation. Recently, the hormonal variabilities and their possible significance in xylem saps and hydathodes have also been described (Aloni et al., 2005; Fletcher & Mader, 2007; Thompson et al., 2007).

d. Enzymatic variability

It is known since pretty long that some proteins are naturally secreted into plant guttation fluid. In the first quarter of the last century, Wilson (1923) reported for the first time, the presence of enzymes catalase and peroxidase in the guttation fluid of maize {Zea mays) and oats (Avena sativa), whereas reductase was released by timothy {Phleum pratense). Recent studies have revealed the presence of a number of proteins and enzymes of immense metabolic significance in guttation water. Shepherd and Wagner (2007) have described the physical structures and biochemistry of the phylloplane proteins. They have also reviewed the emerging evidence pertaining to antimicrobial phylloplane proteins and mechanisms by which proteins can be released to the phylloplane by specific trichomes and delivery in guttation fluid from hydathodes. Similarly, a number of transport proteins have been detected in guttation fluid. Transport studies in cultured Arabidopsis cells indicate that adenine and cytokinin are transported by a common H+-coupled high-affinity purine transport system involving AtPUPI and AtPUP2, transport properties being similar to that of Arabidopsis purine transporters (Burkle et al., 2003). Promoter-reporter gene studies point towards AtPUPI expression in the epithem of hydathodes and the stigma surface of siliques, suggesting a role in retrieval of cytokinins from xylem sap to prevent their loss during guttation. As for sugars particularly glucose, fructose, galactose and sucrose, they have been found in guttation fluid of cereals (Goatley & Lewis, 1966). The data obtained by Slewinski et al., (2009) demonstrate that SUT1 is crucial for efficient phloem loading of sucrose and it may get its way into xylem saps hence guttation, may well be due to inter-trafficking of contents between xylem and phloem tissues in maize leaves. Transporter proteins may be found in guttation fluid for other sugars as well. The mRNA localization in all organ sieves, suggests a role in sap nutrient transport and guttation with kinetic studies showing a pattern similar to that of sucrose content variation (Testone et al., 2009). Thus, large variabilities seem to exist at the enzymatic level influencing guttation among a number of plant activities.

2. External factors

a. Environmental factors

The environmental conditions in general affect root pressure, but because of genetic differences related to internal cellular sensing networks, responses vary between plants in terms of the effect on root pressure. Obviously, conditions that discourage root pressure such as cold, dry aerated soil etc also reduce guttation.

i. Mechanical stimuli

As mentioned earlier, the ability to sense and respond to environmental and physical stimuli through mechanosensory signal is of key importance to all living things. Among the common environmental stimuli detected by living organisms are light, temperature, and a variety of chemical signals. A number of these stimuli appear to be closely related and can be considered as physical-mechanical stimuli, that is, differences in a mechanical force or pressure perceived by the living cell. As stated earlier, a cell may perceive gravity, strains caused by self-loading and internal growth; mechanical loading by snow, ice, fruit; wind, rainfall, touch, sound; and the state of hydration (turgor pressure) within a cell. All organisms appear to perceive these mechanical signals, regardless of their taxonomic classification or life habit. The significant differences between taxonomic groups are found in the individual molecular components of the micro structure of the internal cellular sensing network and in the response of an individual organism to each mechanical stimulus (Baluska et al., 2003; Telewski, 2006; Baluska & Mancuso, 2009; Baluska, 2010). It is therefore, assumed that these natural mechanical stimuli are in some way linked to guttation.

ii. Temperature

Atmospheric temperature is one of the most important environmental factors influencing guttation. Cool nights following warm days provide ideal conditions for guttation as root absorption of water and nutrients continues unabated while transpiration is materially reduced (Kramer & Boyer, 1995). Further, although periodicity in bleeding appears to be automatic in origin, a sharp increase in temperature will determine the time of occurrence of its maxima and minima (Skoog et ah, 1938). The frequent occurrence of guttation during cool spring nights following warm days underlines the importance of warmth for guttation in some plants (Gaumann, 1938). Obviously, guttation being an energy-dependent process as discussed earlier, temperature plays a dominant role in its regulation. Pedersen (1993, 1994) found the acropetal water transport resulting in guttation to be an active process dependent on temperature in submerged aquatic plants. The flow stopped by cooling the root compartment to 4[degrees]C, and lowering the temperature from 15 to 10[degrees]C reduced the guttation rate 5-fold. Interestingly, the activity of water channels is also affected by temperature as aquaporin's activity in plasma membranes is under metabolic control (Mahdieh et ah, 2008).

It is therefore, concluded that temperature plays a decisive role in regulating guttation.

iii. Light

The effect of light on guttation has been studied by several workers (Cochard et al, 2007; Kim & Steudle, 2009). For example, etiolated seedlings of oats exhibit a wave of guttation 3 to 6 h after light strikes them (Mcintyre, 1994). This phenomenon will occur in all wavelengths of light while under continuous light but under darkness no such wave in guttation occurs. Engel and Friederichsen (1954) over a number of years studied this phenomenon in a series of investigations wherein the light-induced wave in guttation was superimposed upon a 24 h endogenous guttation cycle. Light was found to induce a loss of about 30 % in the original length of oat coleoptiles. On the basis of the magnitude of the effect observed, it appears that the light-induced increase in guttation of oat seedlings is brought about by a secretion of water during the shortening of the coleoptile cells and is not directly related to changes in root pressure or bleeding. These authors further observed that the guttation of Zea mays coleoptiles increased when exposed to light with a maximum about two hours after start of illumination, and generally decreased during dark periods. It would be interesting to investigate these aspects of guttation in agricultural and horticultural crops and varieties thereof with the focus on the energetics of mineral nutrients uptake and transport facilitated by membrane ATPases under the influence of various wavelengths of light.

iv. Humidity

High atmospheric humidity is one of the essential prerequisites for guttation fluid to appear. As stated earlier, guttation is ample and continues for a relatively longer period when the soil and atmosphere are saturated with water. If the roots are immersed in a dilute salt solution containing mobile ions, are well-aerated, and kept at a favorable temperature, rapid guttation continues for an extended period of time in humid atmosphere because of very low vapor pressure deficit discouraging transpiration (Hoagland & Broyer, 1936).

v. Wind

Exudation of guttation water by the grass leaves is often noticed when the air is saturated and when there is almost no wind. Typical guttation nights are classically considered to be calm because the wind transports (noctumally) warmer air from higher levels to the cold surface. Recently, Singh et al. (2009a) investigated the effects of some common environmental and edaphic factors such as wind velocity and soil moisture stress on guttation in rice. The volume of exuded fluids from tips of rice leaves declined sharply from 100 [micro]L at 0 rpm down to 75 [micro]L at 30 rpm and only traces of it could be observed at 60 rpm of fan speed during half-an-hour period. This could be due to increased vapor pressure deficit around rice leaves exposed to increasing fan speeds though unfortunately the vapor pressure deficit was not controlled. Thus, the wind velocity appears to play a dominant role in the regulation of guttation and its appearance as droplets.

b. Edaphic factors

i. Soil and root temperature

Guttation being an energy-dependent process as discussed earlier, root temperature plays a dominant role in its regulation. Pedersen (1993, 1994) showed by measuring the rate of guttation that in submerged aquatic plants Sparganium emersum and Lobelia dortmanna the acropetal water transport is clearly an active process confined to the roots. The flow is stopped by cooling the root compartment to 4[degrees]C, and lowering the temperature from 15 to 10[degrees]C reduced the guttation rate 5-fold. This indicates that the water transport is dependent on root metabolism (Fujii & Tanaka, 1957) and also that the driving force is restricted to the roots. Although periodicity in bleeding appears to be automatic in origin, a sharp increase in temperature will determine the time of occurrence of its maxima and minima. When the soil temperature was changed, a "dose response" of guttation was observed (Skoog et al., 1938).

An explanation of the frequent occurrence of guttation during cool spring nights following warm days can be found in the observations relating to the importance of warm soil for guttation in some plants (Gaumann, 1938). Under spring conditions soil temperatures may remain several degrees higher than air temperatures at night. The intense radiation may warm the soil during the day and a rapid cooling of the air at night produces optimal conditions for guttation to occur (Frey-Wyssling, 1941). Tropical areas with humid night air and warm soil also are particularly favorable for rapid guttation. Hughes and Brimblecombe (1994) studied guttation and dew formation in relation to their environmental significance. The authors found that guttation amount was significantly correlated with soil temperature and moisture (P<0.001, [r.sup.2] = 0.874). Thus, the phenomenon of guttation does appear to be affected significantly by prevalent soil and root temperature suggesting the involvement of metabolic control of minerals uptake via membrane ATPases on the one hand, and functioning of aquaporins for water influx into the roots, on the other, affecting guttation.

ii. Soil moisture

Guttation is very common during warm humid nights in plants growing in high soil moisture. These conditions favor low transpiration and high root pressure. Even at night after periods of water stress, absorption may not completely replace the water deficit in the plant and then actual pressures would not be developed in the xylem (Stocking, 1956a). Thus, no guttation was observed under conditions of soil moisture stress (Kramer & Boyer, 1995; Singh et al., 2009a). The root pressure mechanism, as measured by exudation, ceased in Coleus, sunflower, and tomato plants growing in sandy soil when about 45 % of the moisture available to intact plants still remained in the soil. It appears that root pressure probably is not developed in plants growing in soil containing less than about 45 % of the moisture in the range from moisture equivalent to permanent wilting percentage (Zaitseva et al., 1998). If in these instances water is added to the soil guttation soon follows. Further, the addition of polyethylene glycol (MW 400) to the nutrient medium resulted in a reduction of osmotic potential in the root xylem sap; this osmotic adjustment in the xylem was large enough to establish an osmotic gradient for entry of water and caused guttation at a nutrient solution osmotic potential of -480 kPa (Kaufmann and Eckard, 1971). More recently, Singh et al., (2009a) have provided quantitative data on the relationship between soil moisture stress and guttation in rice. The volumes of guttation fluid were 19 [micro]L, 56 [micro]L and 93 [micro]L at leaf water potentials of-100, -50, and -20 kPa (watered), respectively. Lowered water potentials of roots seem to affect the gating as well as distribution of various isofonns of aquaporins (Katsuhara et al., 2008; Maurel et al., 2008; Heinen et al., 2009; Kaldenhoff et al., 2014) inhibiting the entry of water becoming not enough to cause hydrostatic pressure in the roots on the one hand, and cause cavitation and embolism in plants on the other (Holbrook et al., 2001; Brodribb & Holbrook, 2006). It is further possible that lowered leaf water potentials may affect the sensitivity of hydathode pores as well impacting guttation.

iii. Soil nutrients

The state of plant nutrition plays decisive role in the phenomenon of guttation. Observations have been made on the incidence and amount of guttation as affected by various nutrients and their concentration in the substrate. The metabolic activities of roots of intact barley plants were studied by Crafts and Broyer (1938) and Broyer (1951) and the amount of guttation fluid was found to be associated with the nutrients concentration in the translocatory fluid to the shoots. Results showed that when the roots were immersed in distilled water, guttation was very slight or ceased altogether. This was true, even though the water was aerated amply. In dilute salt solution, but without aeration, guttation was also slight. On the other hand, if the roots were immersed in a dilute salt solution and the aeration was good and the temperature favorable, immense guttation took place. Raleigh (1946) observed that tomato plants which were supplied with complete nutrient solution guttated while those in solutions lacking both nitrate and ammonium nitrogen did not guttate. Deficiency of calcium and magnesium causes reduction in guttation. Guttation was more profuse and was induced in a shorter time with nitrate nitrogen than with ammonium nitrogen. He postulated that the cause for this difference may have been the oxygen supplied by the nitrate. On account of agricultural significance, studies on the nature of phytoremediation and phytomining by guttation of toxic elements from metal-enriched soils also deserve in-depth investigations (Ghosh & Singh, 2005; Meagher & Heaton, 2005; Mihucz et al., 2005; Schmidt et al., 2009). Thus, the state of the nutrition of the plant, through its relation to cell activity including gating of aquaporins, hence permeability to water (Kaldenhoff et al., 2014) seems to affect guttation significantly (Schwenke & Wagner, 1992).

iv. Soil aeration

As described earlier, experiments with barley plants showed that, when the roots were immersed in distilled water, guttation was very slight or ceased altogether (Broyer, 1951). This was true, even though the water was aerated amply. In dilute salt solution, but without aeration, guttation was also slight. It is therefore, clear that aeration, though important, functions only if other factors are not limiting. However, it clearly shows the energy-dependency of root metabolism (Fujii & Tanaka, 1957; Pedersen, 1993, 1994), essential for root pressure development resulting in guttation which does not seem to take place in the absence of oxygen (Sze, 1984; Szarek & Trebacz, 1999; Sze et al., 2002).

v. Soil mycorrhizae

A mycorrhiza is a symbiotic association of a fungus with a root system and several fungi may participate in this association. Plants have root hairs and often mycorrhizal fungi at the root surface. Water and mineral uptake is faster when the mycorrhizal fungi are present in association with the roots (Zholkevich, 1991; Dustmamatov et al., 2004). There seems to be a relation between guttation and mycorrhizae content in the soil. There is plenty of evidence for improved nutrient acquisition by ectomycorrhizae in trees; however, their role in water uptake is much less clear (Lehto & Zwiazek, 2011). The clearest direct mechanism for increased water uptake is the increased extension growth and absorbing surface area, particularly in fungal species with external mycelium of the long-distance exploration type such that as much as three meters of fungal hyphae can be extended from each centimeter of root. Some studies have found increased aquaporin function and, consequently, increased root hydraulic conductivity in ectomycorrhizal plants under both well-watered and drought-stressed conditions (Barzana et al., 2012). The aquaporin function of the fungal hyphae is also likely to be important for the uptake of water by the ectomycorrhizal plant, but more work needs to be done in this area. The best-known indirect mechanism for mycorrhizal effects on water relations is improved nutrient status thereby influencing water uptake, root pressure and guttation of the host (Raleigh, 1946). In addition, the ability of arbuscular mycorrhizal symbiotic plants to switch between apoplastic and cell-to-cell water transport pathways could allow a higher flexibility in the response of these plants to the rate of guttation. Obviously, more work is required to illustrate its link to guttation.

Summarily, the effects of important factors that seem to regulate the phenomenon of guttation, have been described. From the array of evidence and discussion presented in this paper it becomes clear that the process of guttation is governed and regulated principally by genetic makeup of the plants, but greatly modified by environmental and edaphic factors the plants are exposed to during their growth and development.

Conclusions and Future Perspectives

This review has highlighted recent advances in guttation research specifically pertaining to its mode, mechanism and regulation. Guttation is known to serve a number of purposes for plants and people and its overall impact now outweighs those earlier envisaged (Singh, 2013; Singh & Singh, 2013; Singh, 2014a, b). Yet, the mechanism underlying this intriguing physiological phenomenon is far from understood though of late, significant advances have been made in its structural biology, physiology, biochemistry, microbiology, phytopathology, and biotechnology. This process, though genetically governed, is triggered and regulated by the interaction of several internal, external and edaphic factors finely-tuned to chemico-mechanosensory network such as mechanical stimuli, i.e. light, temperature, humidity, wind, turgor potential, membrane potential etc on the one hand, and chemical signals received from within and from above- and below-ground plant parts that involve a number of enzymes such as H+-ATPases, kinases, phosphatases and hormones causing and influencing secretion of fluid, i.e. guttation, on the other. Many areas of research however, still remain unresolved and unexplored such as there is need to know why some plant species and genotypes thereof guttate copiously than others. We need to know whether it is the quantity or quality or both of guttate which are significant in impacting plant growth and crop productivity through its contribution to enhanced reproductive sink-potential (Quanzhi et al, 1999; Singh et al., 2008) or in some other way. Are the quantity and quality parameters of guttation fluid independent of each other? We also need to know how precisely the chemico-mechanosensors exert their influence on the phenomenon of guttation. Some initial but fascinating success has been achieved through genetic studies shedding light on the involvement of specific proteins in the regulation of hydathodes development and by gene transfer engineering efforts have been made to unravel the mechanism of secretion of amino acids, drugs and vaccines by hydathodes. These are remarkable achievements as few years ago such ideas could not be experimentally tested. Therefore, there is great potential for progress in understanding the genetic and molecular basis of guttation, e.g. through the production of both gain- and loss-of-function plants adopting model techniques and combinations thereof. The genetics of this phenomenon and QTLs mapping for quantitative and qualitative traits of these fluids are essential and highly desirable which may be aided by modern improved techniques like gene editing, functional magnetic resonance imaging (fMRI), positron emitting technique (PET), required chips and stem cell/tissue culture. It will be extremely important this and over the next decade to work towards the understanding of this phenomenon. Further, how light with effects of its quality exactly triggers the initiation of guttation is another unresolved issue in photobiology. There is need to explore whether hydathodes have system to convert light into electrical signals, if so, how it is achieved. The use of mutants of Arabidopsis thaliana, Oryza sativa and Lycopersicon esculentum, the model plants, may be helpful and rewarding for unraveling the mechanism of guttation. There is a lack of information on varietal differences in guttation among field and horticultural crops including cash crops though the rate of guttation differs widely not only among species but among varieties thereof too. Further, there is also no information on the role of vitamins in guttation or guttation in relation to vitamins in various genotypes of food, feed, fiber and fodder crops. Therefore, such work would be rewarding for developing guttation-efficient cultivars for enhanced biomass and economic yield. Happily, new techniques in cellular, molecular, and genetic biology are opening up vast opportunities for scientists to explore these unresolved issues of guttation. Although scientists may not be able to unravel with total accuracy the mechanism, they are beginning to understand the principles that govern and direct their operation. They may also witness evidence of chaos in models and experiments in guttation research and which is why it is still premature to assume that the full knowledge of the mechanism of exudation would be in sight in near future. I hope that future work on guttation would be exciting, inspiring, fascinating and challenging as it ought to lead to major advances in our fuller understanding of the mechanism of guttation and to useful biotechnological innovations to cater for the human needs under changing society and environment (Sutton et ah, 2007; Tappero et ah, 2007).

Acknowledgments The author expresses his deep sense of gratitude to Mr. Tesfaye Wossen, Head of the Department of Plant Sciences and Mr. Sisay Yehuala, Dean of the College of Agriculture & Rural transformation, University of Gondar, Ethiopia for their continued support and inspiration. My sincere thanks go to the learned anonymous reviewer(s) for critical comments and valuable suggestions for the improvement of the manuscript. I also owe my debt to Prof. Dennis Stevenson, Editor of Botanical Review for giving me opportunity to write this review article.

DOI 10.1007/s12229-016-9165-y

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Sanjay Singh (1,2)

(1) Department of Plant Sciences, College of Agriculture & Rural Transformation, University of Gondar, Gondar City, Ethiopia

(2) Author for Correspondence; e-mail: sanju80gon@gmail.com

Published online: 13 May 2016
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