Quantifying Apoplastic Flux through Red Pine Root Systems Using Trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate

Hanson, Paul J.; Sucoff, Edward; Markhart, Albert H.

doi:10.1104/pp.77.1.21

Cited by 71 publications

(41 citation statements)

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“…The molecule mass of RB is 479 D, higher than that of the water molecule. The rates of transport of fluorescent tracers and water through the apoplast may be different due to their different molecular sizes (Hanson et al, 1985;Yeo et al, 1987). Therefore, the concentration of RB in the xylem sap gives an indication rather than a precise estimate of the ratio of symplastic to apoplastic water transport.…”

Section: Discussionmentioning

confidence: 99%

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

1999

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HgCl 2 (0.1 mM) reduced pressure-induced water flux and root hydraulic conductivity in the roots of 1-year-old aspen (Populus tremuloides Michx.) seedlings by about 50%. The inhibition was reversed with 50 mM mercaptoethanol. Mercurial treatment reduced the activation energy of water transport in the roots from 10.82 ؎ 0.700 kcal mol ؊1 to 6.67 ؎ 0.193 kcal mol ؊1 when measured over the 4°C to 25°C temperature range. An increase in rhodamine B concentration in the xylem sap of mercury-treated roots suggested a decrease in the symplastic transport of water. However, the apoplastic pathway in both control and mercurytreated roots constituted only a small fraction of the total root water transport. Electrical conductivity and osmotic potentials of the expressed xylem sap suggested that 0.1 mM HgCl 2 and temperature changes over the 4°C to 25°C range did not induce cell membrane leakage. The 0.1 mM HgCl 2 solution applied as a root drench severely reduced stomatal conductance in intact plants, and this reduction was partly reversed by 50 mM mercaptoethanol. In excised shoots, 0.1 mM HgCl 2 did not affect stomatal conductance, suggesting that the signal that triggered stomatal closure originated in the roots. We suggest that mercury-sensitive processes in aspen roots play a significant role in regulating plant water balance by their effects on root hydraulic conductivity.Several criteria have been used to infer the presence of water-transporting channels in cell membranes. These include a high ratio of osmotic to diffusional water permeability (P f /P d Ͼ1), low Arrhenius activation energy (E a Ͻ 6 kcal mol Ϫ1 ) for water transport, and its reversible inhibition by mercury sulfhydryl reagents (for reviews, see Chrispeels and Agre, 1994;Verkman et al., 1996;Maurel, 1997). The transport of water through the lipid bilayer has a high E a , usually above 10 kcal mol Ϫ1 (Macey, 1984). Water transport can also be via water channel proteins (aquaporins), which have been found in the tonoplasts (Maurel et al., 1993) and plasma membranes (Kammerloher et al., 1994) of plants. It is generally acknowledged that the transport of water via channels is less temperature dependent and has a lower E a (Ͻ 6 kcal mol Ϫ1 ) than transport via the lipid pathway (Finkelstein, 1987;Chrispeels and Agre, 1994). Water transport via aquaporins is characteristically inhibited by mercurial reagents, which react with sulfhydryl groups in the channel proteins and result in closure of the channels. This closure inhibits water transport and increases E a to the level of that for transport through the lipid pathway (Macey, 1984). An inhibition of water transport by mercury was reported in cell membranes isolated from higher plants Niemietz and Tyerman, 1997) and in whole root systems (Maggio and Joly, 1995;Carvajal et al., 1996). However, the effects of mercury reagents on E a have not been investigated in intact higher plants.Based on the composite transport model (Steudle and Frensch, 1996), water transport is via three parallel pathways, apoplastic, ...

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Section: Discussionmentioning

confidence: 99%

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

1999

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“…15) In rice, apoplastic flow is of major importance in Na þ uptake. 14,16) The apoplastic flow from root to shoot is enough to account for the accumulation of Na þ in the leaves of rice.…”

Section: )mentioning

confidence: 99%

“…14) Apoplastic flow tracers such as the fluorescent compound PTS (8-hydroxy-1,3,6-pyrenetrisulphonic acid) have been used to examine apoplastic flow. 15) In rice, apoplastic flow is of major importance in Na þ uptake. 14,16) The apoplastic flow from root to shoot is enough to account for the accumulation of Na þ in the leaves of rice.…”

mentioning

confidence: 99%

Exogenous Proline and Glycinebetaine Suppress Apoplastic Flow to Reduce Na⁺Uptake in Rice Seedlings

Sobahan

Arias

Okuma

et al. 2009

Bioscience, Biotechnology, and Biochemistry

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The application of exogenous proline and glycinebetaine (betaine) confers salt tolerance on plants under salt stress. The effects of exogenous proline and betaine on apoplastic flow in rice plants under saline conditions were investigated using trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS), an apoplastic tracer. Rice plants took up more PTS under light conditions than under dark conditions. Salt stress increased PTS uptake and Na þ content of rice leaves, but did not affect K þ content, resulting in a lower K þ /Na þ ratio. Addition of proline or betaine to the saline medium suppressed Na þ -induced PTS uptake and Na þ accumulation, while the K þ content was slightly increased, which led to a high K þ /Na þ ratio under saline conditions. These results suggest that exogenous proline and betaine suppressed Na þ -enhanced apoplastic flow to reduce Na þ uptake in rice plants.Key words: apoplastic flow; proline; rice; salt stress; trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS) Salinity is one of the major abiotic stresses that adversely affect crop growth and productivity.1) Since about 20% of irrigated agricultural land is negatively affected by salinity and about 10 Â 10 6 ha of irrigated land are thought to be damaged every year, improvements in the salt tolerance of crops are necessary to increase productivity.2,3) Although salt tolerance mechanisms have not fully been understood, it is thought that the main reasons for losses in higher-plant growth are osmotic damage and ion cytotoxicity. 4)Plant cells maintain osmotic balance using compatible solutes, but salinity causes perturbation of water potential in plant cells. This perturbation leads physiological problems in salt stressed plants because water functions as a solvent, an electron donor in the Hill reaction, and a coolant. 5) Salinity also causes ionic stress, that is, it decreases the ratio of K þ to Na þ in plant cells. 6,7) In addition, salinity causes lipid peroxidation in plant cells, causes many metabolic disturbances in plants, and impairs various enzymatic reactions. [8][9][10][11] Rice, one of most important crops, is moderately sensitive to salinity. 12) In most plants, radial transport of Na þ to the root xylem occurs via a symplastic pathway involving loading transporters, 13) but in rice there is a quite separate route that leads to the passage of salts from roots to leaves and allows accumulation to toxic levels, namely, apoplastic flow.14) Apoplastic flow tracers such as the fluorescent compound PTS (8-hydroxy-1,3,6-pyrenetrisulphonic acid) have been used to examine apoplastic flow. 15) In rice, apoplastic flow is of major importance in Na þ uptake. 14,16) The apoplastic flow from root to shoot is enough to account for the accumulation of Na þ in the leaves of rice. 6,17) Sodium ions increased apoplastic flow and decreased transpiration, in which stomatal movement is closely involved. 18)These results indicate that water can move via the apoplastic pathway and the symplastic and transmembrane pathways.Proline and betai...

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“…However, soil solution can reach the xylem vessels by the apoplasmic pathway at the root tip before the endodermis is fully differentiated or at the sites at which secondary root emergence causes temporary holes in the endodermal apoplasmic barrier (Pitman, 1982). Soil solution that flows to the xylem through the apoplasmic pathway contributes Ͻ1% of the xylem sap volume (Perry and Greenway, 1973;Hanson et al, 1985;Skinner and Radin, 1994), except for in rice, in which it can contribute up to 5.5% (Garcia et al, 1997). Nevertheless, the apoplasmic stream can contribute significantly to the ion concentration of the xylem sap because there is no barrier for the ions conducted in this stream.…”

Section: Shoot Na ؉ Overaccumulation Is Due To An Alteration Of the Rmentioning

confidence: 99%

sas1, an Arabidopsis Mutant Overaccumulating Sodium in the Shoot, Shows Deficiency in the Control of the Root Radial Transport of Sodium

et al. 2001

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A recessive mutation of Arabidopsis designated sas1 (for sodium overaccumulation in shoot) that was mapped to the bottom of chromosome III resulted in a two-to sevenfold overaccumulation of Na ؉ in shoots compared with wild-type plants. sas1 is a pleiotropic mutation that also caused severe growth reduction. The impact of NaCl stress on growth was similar for sas1 and wild-type plants; however, with regard to survival, sas1 plants displayed increased sensitivity to NaCl and LiCl treatments compared with wild-type plants. sas1 mutants overaccumulated Na ؉ and its toxic structural analog Li ؉ , but not K ؉ , Mg 2 ؉ , or Ca 2 ؉ . Sodium accumulated preferentially over K ؉ in a similar manner for sas1 and wild-type plants. Sodium overaccumulation occurred in all of the aerial organs of intact sas1 plants but not in roots. Sodium-treated leaf fragments or calli displayed similar Na ؉ accumulation levels for sas1 and wild-type tissues. This suggested that the sas1 mutation impaired Na ؉ long-distance transport from roots to shoots. The transpiration stream was similar in sas1 and wild-type plants, whereas the Na ؉ concentration in the xylem sap of sas1 plants was 5.5-fold higher than that of wild-type plants. These results suggest that the sas1 mutation disrupts control of the radial transport of Na ؉ from the soil solution to the xylem vessels. INTRODUCTIONAmong abiotic stresses, salinity is one of the major causes of yield losses of crop plants (Boyer, 1982). Salt stress is a polymorphous stress that reduces yield through three direct effects: osmotic stress, nutritional stress, and ion toxicity. It is widely thought that breeding for salt tolerance will involve developing a pyramiding strategy for selecting favorable combinations of traits, each of which would improve one of the physiological adaptations to salt stress (Yeo and Flowers, 1986). However, it is not clear which traits are appropriate for use in breeding programs to improve salt tolerance. Many physiological and molecular responses to salinity have been described (Greenway and Munns, 1980;Munns, 1993;Yeo, 1998), but their effects on the improvement of salt tolerance have seldom been demonstrated. This observation made clear the necessity of developing genetic approaches to establish which responses are physiologically relevant to salt tolerance (Epstein et al., 1980).The contributions of different physiological responses to salt tolerance were analyzed recently in genetic studies with a number of different variants (mutants or transgenic plants). The advantages of using mutants are that no prior knowledge of the molecular bases of the mechanism of interest is necessary and that mutants can reveal mechanisms previously unknown to be involved in salt tolerance. The identification and characterization of salt-tolerant and salt-hypersensitive mutants have drawn attention to several matters: (1) the control of Cl Ϫ transport from root to shoot (Abel, 1969); (2) the overaccumulation of proline (Kueh and Bright, 1982); (3) the overaccumulation of Na ϩ and K ϩ ...

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Quantifying Apoplastic Flux through Red Pine Root Systems Using Trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate

Cited by 71 publications

References 13 publications

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

Exogenous Proline and Glycinebetaine Suppress Apoplastic Flow to Reduce Na⁺Uptake in Rice Seedlings

sas1, an Arabidopsis Mutant Overaccumulating Sodium in the Shoot, Shows Deficiency in the Control of the Root Radial Transport of Sodium

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Quantifying Apoplastic Flux through Red Pine Root Systems Using Trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate

Cited by 71 publications

References 13 publications

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

Mercuric Chloride Effects on Root Water Transport in Aspen Seedlings

Exogenous Proline and Glycinebetaine Suppress Apoplastic Flow to Reduce Na+Uptake in Rice Seedlings

sas1, an Arabidopsis Mutant Overaccumulating Sodium in the Shoot, Shows Deficiency in the Control of the Root Radial Transport of Sodium

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Exogenous Proline and Glycinebetaine Suppress Apoplastic Flow to Reduce Na⁺Uptake in Rice Seedlings