Effects Of Various Minerals And Metals On Plants Biology Essay

5.3 Calcium signaling induced by cold or cooling emphasiss. In transgene Arabidopsis, in which aequorin was targeted to different types of root cells, every bit good as to the whole works, cold-water add-on caused a transeunt rise in [ Ca2+cyt ] ( Kiegle et al. 2000 ) .

The maximal extremum occurred at approx. 15-20 s in all cell types. However, the addition in [ Ca2+cyt ] was lower in the root cells, compared with shoot cells. The largest lift was obtained in the deepest cell type, the pericycle, and the lowest peak degree in the elongation zone. Therefore, it was concluded that the size of the sensed agonist does non make up one’s mind the magnitude of the Ca response. Alternatively, there is a cell-specific response.Calcium kineticss under chilling emphasis were besides investigated in individual mesophyll energids from tomato workss loaded with the Ca specific dye Fura2, AM ( Sebastiani, Lindberg and Vitagliano 1999 ) . The energids were subjected to chilling emphasis ( 10-15A°C ) in a temperature-controlled perfusion chamber.

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The consequences showed that different dynamicss in [ Ca2+cyt ] occurred depending on different resting-calcium degrees. In 84 % of the investigated energids there was an addition in [ Ca2+cyt ] . In 21 % of the reacting energids, the maximal [ Ca2+cyt ] was obtained after 10-20 s, therefore confirming consequences from root cells of Arabidopsis ( Kiegle et al. 2000 ) ; in 11 % of the energids both the addition and lessening in [ Ca2+cyt ] were slower ; and in 32 % a changeless addition of [ Ca2+cyt ] was obtained 1 min after start of temperature lessening. When the resting Ca concentration was higher than usually, the addition in [ Ca2+cyt ] was changeless. In these experiments the chilling rate was changeless because a perfusion system was used.

Therefore, it is likely that different cells have different competency and ability to keep calcium homeostasis. A sustained high [ Ca2+cyt ] is implicated in programmed cell death, and in allergic responses to pathogens ( Levine et al. 1996 ) .When a cold solution ( 5oC ) was added to mesophyll energids of wheat foliages, much larger alterations in [ Ca2+cyt ] were obtained than in chilling sensitive tomato energids, in which a perfusion system was used ( Lindberg, Sebastini and Vitagliano 1999, Fig 2 ) . A 2nd add-on of cold solution to the same wheat energid induced different Ca2+cyt dynamicss. The first add-on of cold solution gave a transient drawn-out addition of [ Ca2+cyt ] , which was much smaller than that induced by a 2nd add-on ( Figure 2A, B ) . The 2nd add-on gave a peak response and, thenceforth, a drawn-out Ca addition ( Fig 1B ) . These consequences can non be compared with consequences shown by Knight, Trewavas and Knight ( 1996 ) , since these writers report a mean of 3 or more cold add-ons at clip nothing.

When the wheat energids were treated with erythrosine B, an inhibitor of Ca2+ATPase in the ER and plasma membrane, the Ca transient was prolonged and the magnitude was much higher than without the inhibitor ( Fig 2C ) . Therefore, it is likely that the Ca2+ATPase is involved in the signaling by pumping Ca2+ out from the cytosol.It has been proposed that the [ Ca2+cyt ] signatures are modified by old experience, which means that the works has a Ca “ memory ” ( Knight, Trewavas and Knight 1996 ) . The magnitude of [ Ca2+cyt ] lift elicited by air current becomes increasingly smaller upon repeated stimulation and for some stimulus several hours are needed for a 2nd reaction to take topographic point ( Tuteja and Mahajan 2007 ) . The Ca signature can besides be modified during a 2nd exposure to a emphasis as shown in Figure 1. Furthermore, the magnitude of [ Ca2+cyt ] addition can be changed by anterior in vivo exposure to a contrasting emphasis. These observations imply a cross talk between the signaling Cascadess.

Cold-shock responses were compared in chilling-sensitive baccy and chilling-tolerant Arabidopsis ( Knight, Trewavas and Knight 1996 ) . In both instances an immediate rise in [ Ca2+cyt ] was obtained. In Arabidopsis both EGTA and La caused a partial suppression of [ Ca2+cyt ] and of cold-dependent kin1 cistron look. To look into if the vacuole was involved in the Ca signaling, aequorin was targeted to the cytosolic face of the tonoplast.

The consequences showed that a higher extremum of Ca lift was obtained in the cytosol than in the tonoplast micro-domain. In add-on, the lift in the microdomain, [ Ca2+mic ] , was maintained for a longer clip than the [ Ca2+cyt ] . Pretreatment with fradicin or Li, which interferes with phophoinositide cycling, diminished the Ca reactions, demoing that some outflow of Ca occurred from the vacuoles.

The magnitude of the cold-shock induced [ Ca2+cyt ] response was similar in Arabidopsis and baccy, but was more drawn-out in baccy. Upon insistent add-on of cold solution, the response after 3 and 10 min was weaker in both species. However, baccy was able to retrieve its ability to react to the full to cold daze 30 min after the initial daze, whereas Arabidopsis was non. Another difference between the species was that they responded in different manner to cold daze after acclimatization. Merely in chilling-tolerant Arabidopsis cold acclimatization altered the signature of [ Ca2+ ] cyt, so that cold daze caused a decreased extremum but a drawn-out profile.

The different mechanisms in emphasis response could depend on the different sensitiveness of Arabidopsis and baccy to chilling emphasis. Cold dazes of different amplitude applied to energids of freeze-sensitive olive tree caused transeunt additions in [ Ca2+cyt ] which differed in non-acclimated and acclimated energids ( D’Angeli, Malho and Altamura 2003 ) . Upon repeated cold-shock interventions the transient additions in [ Ca2+ ] cyt were merely reduced when utilizing non-severe rate alterations in temperature. In the acclimated protoplasts the [ Ca2+ ] cyt lifts were farther reduced.Temperature feeling in Arabidopsis depends both on the chilling rate ( Plieth et al. 1999 ) and the concluding temperature to which chilling occurs ( Knight 2002 ) .

Plieth ( 1999 ) presented a mathematical theoretical account of how cold is sensed by a works based on a inactive inflow across the plasma membrane and an active outflow by a pump. A individual extremum in [ Ca2+cyt ] is obtained with a cold daze, that is, at a really fast temperature lessening, but at low chilling rate, the response lacks the initial extremum more or less. The pump slows down at low temperature taking to a 2nd slow stage of the addition in [ Ca2+cyt ] . A biphasic response to a individual chilling measure is therefore obtained when the sensitising action by the temperature alteration on the pumps and channels are of equal magnitude ( Plieth 1999 ) .ABy using spot clinch technique to Arabidopsis mesophyll cells, Carpaneto et Al. ( 2007 ) showed that cold induced a rapid addition in [ Ca2+cyt ] , and that the inflow of Ca could happen through non-selective cation channels.5.

4 Cold daze induces alterations in the membrane potencyA bead in temperature could besides alter the trans membrane possible. Krol, Dziubinska and Trebacz ( 2004 ) showed that the obtained transeunt depolarisation of membrane potency in mesophyll cells of Arabidopsis, Helianthus and Vicea, induced by temperature lessening, depended on Ca inflow from both apoplast and internal shops. It was verified subsequently that the cold-induced depolarisations depended on Ca inflow ( Carpaneto et al. 2007 ) . Verapamil, a Ca channel blocker, caused important suppression of the cold-induced possible alterations. Since the presence of calmodulin adversaries prolonged the repolarization, this could be attributed to activation of CaM-dependent Ca2+-ATPases ( Krol, Dziubinska and Trebacz ( 2004 ) . It was reported that this enzyme is involved in low temperature response in rice ( Martin and Busconi 2001 ) .

A suggested theoretical account for cold signaling in workss is shown in Fig. 3.6. Salt ; Sodium and osmotic emphasis signalingSoil salt is a major environmental jeopardy worldwide as more than 40 % of the Earth is waterless or semi-arid and most of the planet ‘s H2O is saline. Presently more than 6 % of the universe ‘s land, which exceeds 20 % if merely the irrigated country is considered, is affected by changing grades of dirt salt ( Flowers and Yeo 1995, Munns 2002, Kader and Lindberg 2008 ) . However, about 50 per centum of the irrigated land is in the waterless and semi-arid parts of the universe, and is confronting most serious salt jobs.6.

1 Salinity emphasis has an impact on agricultural productivenessSalinity emphasis adversely affects agricultural productiveness by diminishing the harvest output in many ways. Furthermore, the saline country additions twenty-four hours by twenty-four hours due to low-lying rise and, therefore, will hold profound harmful effects on agricultural productiveness in many states of the universe. Long clip ago Buringh ( 1979 ) estimated that at least 10 hectares of cultivable land are lost from the agricultural production in every minute, of which three hectares are lost due to dirty salinization. In 2002, FAO reported that about 20-30 million hectares of irrigated land were earnestly damaged by the build-up of salts and 0.

25-0.50 million hectares were to be lost from production every twelvemonth as a consequence of salt build-up ( Martinez-Beltran and Manzur 2005 ) . The black effect of this increasing salt emphasis together with the turning universe population is surely endangering the hereafter stable planetary nutrient handiness. Agricultural productiveness in the hereafter will largely depend on our ability to place or develop salt-tolerant harvest workss and to turn them in quickly increasing salt-affected lands.6.

2 Salinity stress hurt in workssThe NaCl-dominated salt in nature imposes two primary harmful effects on workss: one is osmotic emphasis and the other one is ionic toxicity. Due to the presence of high salt, salt emphasis increases the osmotic force per unit area in the dirt solution over the osmotic force per unit area in works cells. As a consequence, works loses its ability for consumption of H2O and minerals, particularly the consumption of K+ and Ca2+ ( Glenn, Brown and Kahn 1997, Munns, James and Lauchli 2006 ) . Plant growing suppression by high sums of Na+ and Cl- is one of the chief hurtful effects of salt emphasis. When present in extra sum, Na+ and Cl- ions can come in into the works cells and exert toxic effects on cell membranes, and on metabolic activities in the cytosolic portion of the cell ( Greenway and Munns 1980, Hasegawa et Al. 2000, Zhu 2001 ) . The attendant consequence of osmotic emphasis and ionic toxicity may take to secondary effects in workss such as reduced cell enlargement, production of assimilate and membrane maps, decreased cytosolic metamorphosis and raised production of reactive O intermediates ( ROSs ) .

A6.3 Salinity emphasis tolerance mechanisms in workssAs paleontological and molecular grounds suggest, the embryophytes ( tellurian workss that are non algae ) were evolved from the Streptophyta some 500 million old ages ago ( Raven and Edwards 2001 ) . The development of salt tolerance mechanisms in halophytic workss has late been reviewed by Flowers, Galal and Bromham ( 2010a ) . Though physiological foundations of salt tolerance are present in all workss, works species show a really broad scope of adaptability to salt emphasis. For illustration, glycophytes like garbanzo is really sensitive to salt emphasis, and suffer toxicity at merely 25 millimeters NaCl ( Flowers et Al.

2010b ) , whereas halophytes can digest salt concentration every bit high as 1000 millimeter ( Khan, Ungar and Showalter 2005 ) . The recent promotion in molecular biological science research is bring outing the mechanisms of salt emphasis tolerance including the cardinal cistrons involved in the molecular webs and the signaling cascade that mediates works responses to salt emphasis. Since salt emphasis elicits two different inauspicious effects like osmotic emphasis and ionic toxicity in workss, workss need different tolerance mechanisms to be adopted under this emphasis. To cover with the ionic toxicity under NaCl-dominated salt emphasis the key mechanisms for tolerance are a lessened toxic ion consumption into the cytosol, ability to restrict the entry of these toxic ions into the transpiration watercourse, the ability to modulate transpiration in the presence of these toxic ions and compartmentalisation of Na+ and Cl- ions in to the apoplast, or into the vacuole ( Blumwald 2000, Tester and Davenport 2003, Kader and Lindberg 2005, Kader and Lindberg 2008, Munns and Tester, 2008, Flowers and Colmer 2008, Flowers, Galal and Bromham 2010a ) . Compartmentalization of toxic Na+ into the vacuole is advantageous, since it is no more toxic for the cell, and besides a benefit both for growing and for accommodation of the osmotic potency ( Flowers and Lauchli 1983, Jhu 2003, Subbarao et Al.

2003, RodrA?guez-Navarro and Rubio 2006 ) .A Jou et Al. ( 2006 ) showed that extra Na+ besides can be compartmentalized in ER and Golgi organic structures.An of import tolerance mechanism is besides a works ‘s capableness to increase the consumption of K, K+ , and to diminish the consumption of Na+ into the cytosol under high Na concentration. Expression analyses of transporter cistrons for K+ and Na+ transporters OsHKT1 and OsHKT2 showed that they were otherwise expressed in tolerant and sensitive rice cultivars ( Kader et al.

2006 ) .To obtain osmotic homeostasis the synthesis of compitable organic solutes, like glycine betaine, Osmitrol, pinitol, proline, sorbitol, sucrose and trehalose in the cytosol is of importance ( Bohnert and Jensen 1996, Chen and Murata 2002, Zhu 2002, Zhang, Creelman and Zhu 2004, Chinnusamy, Jagendorf and Zhu 2005, Taiz and Zeiger 2006, Liang et Al. 2009 ) .6.4 Percept of salt emphasis in workssCellular perceptual experience of salt emphasis by workss is prerequisite to get down the activation of the whole cell-signaling cascade. This begins with an lift of [ Ca2+ ] cyt and ends with different tolerance mechanisms activated in the works. Like other emphasiss, salt emphasis ( both osmotic emphasis and ionic toxicity ) is perceived in workss at the cell membrane, either extra-cellularly or intra-cellularly by a protein crossing the plasma membrane and/or an enzyme within the cytosol ( Zhu 2003 ) . Under salt emphasis, a low K+ degree in the cytosol may besides take to cytosolic Ca signals ( Luan, Lan and Lee 2009 ) .

For feeling the osmotic constituent of salt emphasis, several detectors likely are involved ( Urao et al. 1999, Reiser, Raitt and Saito 2003, Tamura et Al. 2003, Boudsocq and Lauriere 2005, Tran et Al.

2007, Wohlbach, Quirino and Sussmand 2008 ) . A significant advancement in understanding the signal transduction under Na+ toxicity was made by designation of the Salt Overly Sensitive ( SOS ) tract in Arabidopsis ( Zhu, 2002 ) . In a recent reappraisal Luan, Lan and Lee ( 2009 ) suggested that CBL ( calcineurin B-like proteins ) -CIPK ( CBL-interacting protein kinase ) pathways modulate Na+ conveyance in workss and therefore confabulate salt tolerance. The CBLs besides appear to be an of import group for confabulating salt tolerance through enhanced K+ uptake under salt emphasis ( Luan, Lan and Lee 2009 ) . As shown in Fig. 4, the salt tolerance mechanisms in workss entails SOS3, a Ca2+ detector in the cytosol, that reads the alterations in [ Ca2+ ] cyt under salt emphasis and specifically binds Ca2+ . Then this protein interacts with a SOS2 protein kinase. Thereafter, the SOS3-SOS2 composite in bend activates the plasma membrane Na+/H+ antiporter, the SOS1 protein, and re-establish the Na+ homeostasis of the cells.

An lift of [ Ca2+ ] cyt is besides detected by CBL10, which in interaction with SOS2 might trip tonoplast Na+/H+ antiporter to transport Na+ from cytosol to vacuole. Furthermore, the addition in [ Ca2+ ] cyt can besides be perceived by CBL1 and CBL9, which so bind to CIPK23 and interact with the C-terminus of AKT1. In this manner the AKT1 channel is activated doing an increased K+ uptake into the cell, which besides confers salt tolerance.However, it is still necessary to clear up how Na+ toxicity is sensed by the works cell. It was suggested that the SOS1 protein, with its long C-terminal tail in the cytosol, might feel NA+ ( Zhu, 2003, Zhang, Creelman and Zhu 2004, Shabala et al. , 2005 ) .

Kader et Al. ( 2007 ) showed that for Na+ feeling in rice energids, Na+ foremost must come in in to the cytosol. The consequences corroborate the earlier suggestion that the cytosolic tail of the SOS1 protein might feel Na+ . On the other manus, in the halophytic works Cydonia oblonga, Na+ entry in to the cell was non necessary for the displacement in cytosolic Ca2+ ( D’Onofrio and Lindberg, 2009 ) . Therefore, the inquiry still remains to be answered refering the detectors for Na+ toxicity in workss, and if they differ in different species, and/or in salinity-sensitive and salt tolerant cultivars.6.

5 Cytosolic Ca signaling in workss under salt emphasisIt is obviously clear that the salinity-stress perceptual experience, irrespective of how the emphasis is perceived, triggers an intracellular signaling cascade get downing with the lift of secondary courier molecules like Ca in the works cytosol [ Ca2+ ] cyt. Many surveies were done to mensurate the [ Ca2+ ] cyt alterations in cells, variety meats or integral workss under salt emphasis by usage of different techniques. Fluorescence microscopy measurings were performed in root hairs ( Halperin, Gilroy and Lynch 2003 ) and in single mesophyll energids ( Kader et al. 2007, D’Onofrio and Lindberg 2009 ) Measurements in integral whole workss were made by aequorin luminescence sensing ( Knight, Trewavas and Knight 1997, Gao et Al. 2004, Henriksson and Henriksson 2005, Tracy et al.

2008 ) . These surveies suggest that the “ signature ” of [ Ca2+ ] cyt alteration, e.g. the amplitude, continuance and frequence, is really of import for transferring of specific downstream reactions taking to emphasize tolerance.6.6 The signature of cytosolic Ca [ Ca2+ ] cyt differsThe alteration in [ Ca2+ ] cyt varies with species, cell type or tissue type and besides with different techniques used ( Cramer and Jones 1996, Kiegle et Al.

2000, Kader et Al. 2007, Tracy et al. 2008, D’Onofrio and Lindberg, 2009 ) . The alteration in [ Ca2+ ] cyt activates different downstream reactions, such as up-regulation or down-regulation of different cistrons.

The reactions besides may alter with the peculiar emphasis ( Kiegle et al. 2000 ) , the emphasis development rate ( Plieth et al. 1999 ) , Tracy et al. 2008, D’Onofrio and Lindberg 2009 ) , and pre-exposure to the emphasis ( Knight, Trewavas and Knight 1997 ) and the tissue type ( Kiegle et al. 2000 ) , Tracy et al. 2008 ) . Upon application of 100 millimeters NaCl to root cells of Arabidopsis ( Cramer and Jones 1996, Halperin, Gilroy and Lynch 2003 ) , or to maize root energid ( Lynch and Lauchli 1988 ) , a lessening in [ Ca2+ ] cyt was obtained. On the other manus, most surveies show an addition in [ Ca2+ ] cyt upon salt emphasis ( Bittisnich, Robinson and Whitecross 1989, Lynch, Polito and Laˆzuchli 1989, Knight, Trewavas and Knight 1997, Halfter, Ishitani and Zhu 2000, Kiegle et Al.

2000, Knight 2000, Zhu 2001, Gao et Al. 2004, Henrikson and Henrikson 2005, Kader et Al. 2007, D’Onofrio and Lindberg, 2009A6.

7 Plant roots and shoots signal differentially under Na toxicity and osmotic emphasis.Contrasting consequences are reported whether osmotic emphasis additions or lessenings [ Ca2+ ] cyt ( Cramer and Jones 1996 ; Knight, Trewavas and Knight 1997, Kiegle et Al. 2000, Kader et Al. 2007 ) . Osmotic and ionic emphasiss induced different displacements in [ Ca2+ ] cyt in Arabidopsis root cells and the heterogeneous [ Ca2+ ] cyt alterations were found merely in the root ( Tracy et al. 2008 ) . Besides in experiments with rice and Cydonia oblonga energids, different [ Ca2+ ] cyt alterations were induced under Na emphasis and under osmotic emphasis ( Kader et al.

2007, D’Onofrio and Lindberg 2009 ) .A proposed theoretical account for Ca and pH-signaling under salt emphasis is reviewed in Kader and Lindberg ( 2008, 2010 ) .7.

Aluminum and heavy metal emphasis signaling in workss7.1 Aluminium toxicity to workssAluminium ( Al ) toxicity in workss is a serious factor restricting harvest production in acidic dirts, impacting up to 40 % of the universe ‘s cultivable dirts ( Haug 1984, Foy 1984 ) . When the dirt pH decreases below 5, Al3+ is solved in the dirt, doing harmful effects on works roots. At pH 4 the dominating species is Al ( H2O ) 3+ ; at higher pH besides Al ( OH ) 2+ , Al ( OH ) 2+ , Al ( OH ) 30 and Al ( OH ) 4- are present, besides sulfate composites and polynuclear species ( Lindsay 1979 ) .When roots are subjected to Al they become scrawny and damaged and root hair development is hapless ( Clarkson 1965 ) .

The consumption of H2O and minerals is badly inhibited.At a low pH Al chiefly binds to the root vertex and inhibits root elongation ( Ryan, DiTomaso and Kochian 1993, Kochian 1995, Matsomoto 2000, Barcelo and Poschenrieder 2002 ) . Aluminum affects the transmembrane potency of root cells and inhibits ATPase activities. After cultivation of sugar Beta vulgariss in the presence of low pH and/or AlCl3, the transmembrane potency, PD, between the vacuole and external medium, PDv, of root cells was mostly depolarized ( Lindberg, Szynkier and Greger 1991 ) . Since the consequence of dinitrophenol was negligable, it was suggested that Al interacts with the active constituent of the PD.

This was confirmed by experiments demoing that Al inhibits the plasma membrane ATPase activity ( Lindberg and Griffiths 1993 ) every bit good as proton conveyance ( Matsumoto 1988 ) . Lipid analysis of sugar Beta vulgaris plasma membranes showed that Al intervention during cultivation caused an addition in the ratio of phoshatidylcholine: phosphatidylethanolamine ( Lindberg and Griffiths 1993 ) . The lipid alterations correlated with the ascertained alteration in the Km for the MgATPase, and, hence, it was concluded that Al could adhere to the membrane-bound enzyme and/or modify the lipid environment.

The suppression of the ATPase activity causes a decreased consumption of minerals. In the dirt, phosphate can precipitate with Al and do phosphate lack in workss ( Horst, Wager and Marschner 1982 )The in vivo and in vitro effects of Al differ. Addition of low concentrations of Al ( 10-50 ?M ) to works roots cultivated without Al caused a fast hyperpolarization of PDv, and of PDc, the membrane potency across the plasma membrane. A depolarisation of PDc was merely obtained at pH 6.

5 ( Lindberg, Szynkier and Greger 1991 ) . At the latter pH the dominant species is Al ( OH ) 30, which is uncharged and can easy perforate membranes. It was shown utilizing unreal liposome cysts that Al consumption was facilitated at impersonal pH, compared with pH 4 and 5 ( Shi and Haug 1988 ) . Therefore, toxic effects of Al on workss can happen besides at a impersonal pH.

Most of the Al binds to the cell walls of root epidermal and cortical cells ( Delhaize, Ryan and Randall 1993 ) and to the plasma membranes, but it can besides perforate the plasma membrane ( Lazof et al. 1994 ) . When Al enters into a cell cytosol it can suppress cell division in the meristem, and cell elongation in the elongation zone ( Baluska, Parker and Barlow 1993 ) likely by adhering to nucleic acids ( Matsumoto et al. 1976 ) .

A7.2 Aluminium interferes with Ca homeostasisA break of cytosolic Ca homeostasis is a primary trigger of Al toxicity. Calcium plays an of import function in cell division and cell enlargement. For case, transeunt alterations in the cytosolic Ca concentration, [ Ca2+cyt ] , have been observed to attach to the mitotic mechanism ( Hepler 1994 ) . Calcium promotes elongation in many works cells ( Takahashi, Scott and Suge 1992, Levina et Al. 1995 ) and calcium adversaries can barricade elongation ( Cho and Hong 1995 ) .

Expansion of tip-growing works cells, such as pollen tubings, is depending on sustained gradients in Ca2+cyt ( Clarkson, Brownlee and Ayling 1988, Felle and Hepler 1997, Wymer, Bibikova and Gilroy 1997 ) . A kept up homeostatic control is, hence, necessary for cell viability ( Bush 1995 ) .AAluminum affects the Ca homeostasis in a cell by suppression of Ca consumption or outflow ( Lindberg 1990 ) . In 1-h experiments with integral sugar Beta vulgaris workss both the metabolic inflow of 45Ca2+ and K+ ( 86Rb+ ) , and the outflow of 45Ca2+ were inhibited in the presence of Al ( Lindberg 1990 ) . Aluminum at a low concentration and low pH can promote the [ Ca2+cyt ] ( Lindberg and Strid 1997 ) .

Aluminum may besides interact with the phosphoinositide signaling tract. Both AlCl3 and Al-citrate inhibited the phospholipid C ( PLC ) action in a dose-dependent mode ( Jones and Kochian 1995 ) .


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