Growth and Accumulation of Solutes by Phytophthora cinnamomi and Other Lower Fungi in Response to Changes in External Osmotic Potential

Luard, Elizabeth J.

doi:10.1099/00221287-128-11-2583

Cited by 20 publications

(21 citation statements)

References 17 publications

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“…Proline, like other compatible osmolytes, is highly soluble and even at concentrations of 1 M or more, does not inhibit enzyme activity or other aspects of cellular metabolism (Jennings and Lysek, 1999). In P. cinnamomi hyphae, proline accumulates as the steady-state external osmotic potential decreases or after hyperosmotic shock and is lost following hypoosmotic shock (Luard, 1982). Together with the earlier measurements of amino acid content in Phytophthora (Luard, 1982;Grant et al, 1988), the present study gives evidence that proline is an important compatible osmolyte in the oomycetes.…”

Section: Discussionmentioning

confidence: 73%

The Role of Proline in Osmoregulation in Phytophthora nicotianae

Ambikapathy

Marshall

Hocart

et al. 2002

Fungal Genetics and Biology

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Section: Discussionmentioning

confidence: 73%

The Role of Proline in Osmoregulation in Phytophthora nicotianae

Ambikapathy

Marshall

Hocart

et al. 2002

Fungal Genetics and Biology

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“…The counterions to K+ and Na+ were assumed to be found in part among the amino acids and other metabolites and in part among macromolecules with negligible osmotic contributions. Chloride was not considered an important counterion, since it generally gives little contribution to the intracellular osmotic potential of fungi (10,22,23). The turgor pressure, which was calculated as the difference between the internal and the external osmotic pressures, showed only little variation with growth rate, giving an average value and standard deviation of 2,200 ± 100 kPa in 4 mM NaCl medium.…”

Section: Resultsmentioning

confidence: 97%

Osmoregulation of the salt-tolerant yeast Debaryomyces hansenii grown in a chemostat at different salinities

et al. 1990

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The intracellular solute composition of the salt-tolerant yeast Debaryomyces hansenii was studied in glucose-limited chemostat cultures at different concentrations of NaCl (4 mM, 0.68 M, and 1.35 M). A strong positive correlation between the total intracellular polyol concentration (glycerol and arabinitol) and medium salinity was demonstrated. The intracellular polyol concentration'was sufficient to balance about 75% of the osmotic pressure of the medium in cultures with 0.68 and 1.35'M NaCl. The intracellular concentration of K+ and Na+, which at low external salinity gave a considerable contribution to the intracellular water potential, was only slightly enhanced with raised medium salinity. However, the ratio of intracellular K+ to Na+ decreased; but this decrease was less drastic in the cells than in the surrounding medium, i.e., the cells were able to select for K+ in favor of Na+. The turgor pressure, which was estimated on the basis of intracellular solute concentrations, was 2,200 kPa in cultures with 4 mM NaCl and decreased when the external salinity was raised, resulting in a value of about 500 kPa in cultures with 1.35 M NaCl. The maintenance of a positive'turgor pressure at high salinity was mainly due to an increased production and accumulation of glycerol.Microorganisms differ in their tolerances to osmotic stress, but in general yeasts and fungi are more tolerant than bacteria (6). Among yeasts, strains of Debaryomyces hansenii and Saccharomyces rouxii are highly osmotolerant and capable of growth in media containing up to about 4 M NaCl (26, 29), whereas Saccharomyces cerevisiae is limited by NaCl concentrations above 1.7 M (29).One of the problems associated with growth in highsalinity media is the establishment of a positive turgor pressure, which is considered to provide the mechanical force for expansion of the cell wall during growth (18,21 When D. hansenii was subjected to increased NaCl stress, there was a decrease of intracellular K+ and an increase of intracellular Na+ (27,28). However, the total salt level in the cells was not sufficient to balance the water potential of the medium; this is why there must be additional osmotically active solutes (28). Many eucaryotic microorganisms accumulate polyols intracellularly when exposed to osmotic stress (1,6,7,15,24), and in D. hansenii a positive correlation was demonstrated between the internal glycerol level and the salinity of the surrounding medium (1, 3). It was also observed that the tolerance for a sudden osmotic dehydration was better in cells having an increased amount of intracellular polyols (2). The two polyols produced and accumulated by D. hansenii are glycerol, which is the major internal solute in exponentially growing cells, and arabinitol, which predominates in stationary-phase cells (2). (8), and at the flow rate used an effective flowthrough cell volume of 0.39 ml was obtained. The culture was pumped at a rate of 80 ml/h from the growth vessel by a peristaltic pump (Microperpex LKB 2132) to a T connection outside the cal...

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“…Likewise, organisms subjected to sustained osmotic stress generally exhibit elevated cellular solute concentrations. Within the fungi there are numerous reports of compatible solute synthesis (17,(19)(20)(21); Phytophthora and Pythium, oomycetes like Achlya, accumulate proline when the external osmotic pressure is raised with sucrose or KCl (17). Achlya displays an alternative strategy: it does not regulate turgor in the short or the long term but extends despite the reduced pressure.…”

Section: Discussionmentioning

confidence: 99%

Extension growth of the water mold Achlya: interplay of turgor and wall strength.

Money

Harold

1992

Proc. Natl. Acad. Sci. U.S.A.

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When hyphae of the water mold Achlya were subjected to osmotic stress, imposed with polyethylene glycol (PEG)-300 or sucrose, turgor pressure fell in proportion to the increase in external osmotic pressure. There was no evidence of turgor regulation, even over a period of days, yet the extension rate was unaffected until turgor was reduced to less than a third of the normal level of 0.6-0.8 MPa (6-8 bars). Measurements of the pressure at which the hyphae burst indicate that they respond to osmotic stress by softening their apical cell walls, sustaining extension growth despite reduced turgor pressure.The effect of osmolytes excluded by the wall was very different; superfusion ofgrowing hyphae with PEG-6000 or dextran-6000 reduced turgor and stopped extension but did not induce wall softenig. Furthermore, the hyphae did not resume growth during an hour or more of continuous exposure to these substances. Although the two classes of osmolytes have the same effect on turgor, they may induce different strains within the cell wall; this might then affect the capacity of the organism to detect the drop in turgor or to soften its cell wall. The interplay between turgor and wall strength supports the proposition that turgor supplies the driving force for extension and that production of the standard hyphal form requires a balance between hydrostatic pressure and a resistive cell wall.Most plant and microbial cells are highly pressurized structures whose walls withstand the tension exerted by up to 2.0 MPa (20 bars) of hydrostatic pressure (1-3). This pressure, or turgor, is generated by water influx due to the difference in osmotic pressure between the protoplasm and the external milieu. Turgor provides skeletal support and, so it is thought, the driving force for expansion. Biophysical models suggest that turgor exerts an isotropic force upon the inner surface of the cell wall, and localized compliance results in the generation of cellular form (4-7).Many organisms, both prokaryotes and eukaryotes, respond to osmotic stress by the accumulation of compatible solutes (1, 3, 8-10), either by synthesis or by uptake from the external medium. The resumption of growth parallels solute accumulation; although few experiments have measured changes in total solute concentration, it seems likely that turgor is rebuilt under these conditions. These studies indicate that turgor is necessary for the growth of walled cells but do not identify its role in the manifold processes that underlie surface expansion.The lower eukaryote Achlya is a convenient subject for investigations on the role of turgor in apical growth; it produces relatively large aseptate hyphae that lend themselves to direct measurement of turgor with a micropipetbased pressure probe (11). We report here that hyphae of Achlya lack a mechanism for turgor regulation but instead sustain apical growth with reduced turgor by softening their cell walls. Our observations reinforce the view that turgor supplies the mechanical force for extension and provide some insight...

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Growth and Accumulation of Solutes by Phytophthora cinnamomi and Other Lower Fungi in Response to Changes in External Osmotic Potential

Cited by 20 publications

References 17 publications

The Role of Proline in Osmoregulation in Phytophthora nicotianae

The Role of Proline in Osmoregulation in Phytophthora nicotianae

Osmoregulation of the salt-tolerant yeast Debaryomyces hansenii grown in a chemostat at different salinities

Extension growth of the water mold Achlya: interplay of turgor and wall strength.

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