Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator.

Verbruggen, Nathalie; Hua, Xuejun; May, Mike; Montagu, Marc Van

doi:10.1073/pnas.93.16.8787

Cited by 178 publications

(184 citation statements)

References 27 publications

(28 reference statements)

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“…Pro catabolism is catalyzed by Pro dehydrogenase and P5C dehydrogenase (Hu et al, 1996;Peng et al, 1996). Suppression of Pro degradation has been demonstrated both in radiolabeling studies (Stewart and Boggess, 1978) and gene expression experiments (Kiyosue et al, 1996;Peng et al, 1996;Verbruggen et al, 1996). Recent studies have demonstrated that high Pro concentrations are present in the phloem sap of drought-stressed alfalfa (Girousse et al, 1996) and that the expression of a Pro-specific amino acid transporter is induced in response to water deficit and salt stress (Rentsch et al, 1996).…”

Section: Discussionmentioning

confidence: 99%

Removal of Feedback Inhibition of Δ1-Pyrroline-5-Carboxylate Synthetase Results in Increased Proline Accumulation and Protection of Plants from Osmotic Stress

et al. 2000

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The ⌬ 1 -pyrroline-5-carboxylate synthetase (P5CS; EC not assigned) is the rate-limiting enzyme in proline (Pro) biosynthesis in plants and is subject to feedback inhibition by Pro. It has been suggested that the feedback regulation of P5CS is lost in plants under stress conditions. We compared Pro levels in transgenic tobacco (Nicotiana tabacum) plants expressing a wild-type form of Vigna aconitifolia P5CS and a mutated form of the enzyme (P5CSF129A) whose feedback inhibition by Pro was removed by site-directed mutagenesis. Transgenic plants expressing P5CSF129A accumulated about 2-fold more Pro than the plants expressing V. aconitifolia wild-type P5CS. This difference was further increased in plants treated with 200 mM NaCl. These results demonstrated that the feedback regulation of P5CS plays a role in controlling the level of Pro in plants under both normal and stress conditions. The elevated Pro also reduced free radical levels in response to osmotic stress, as measured by malondialdehyde production, and significantly improved the ability of the transgenic seedlings to grow in medium containing up to 200 mM NaCl. These findings shed new light on the regulation of Pro biosynthesis in plants and the role of Pro in reducing oxidative stress induced by osmotic stress, in addition to its accepted role as an osmolyte.

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Section: Discussionmentioning

confidence: 99%

Removal of Feedback Inhibition of Δ1-Pyrroline-5-Carboxylate Synthetase Results in Increased Proline Accumulation and Protection of Plants from Osmotic Stress

et al. 2000

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“…2). By comparison, all known reports on de novo synthesis of compatible solutes refer to time scale of several hours (Wyn Jones and Pritchard, 1989;Verbruggen et al, 1996) to days (Kishor et al, 1995). On the other hand, osmotically induced changes in the transcript level of some genes may occur relatively quickly.…”

Section: Discussionmentioning

confidence: 99%

Turgor Regulation in Osmotically Stressed Arabidopsis Epidermal Root Cells. Direct Support for the Role of Inorganic Ion Uptake as Revealed by Concurrent Flux and Cell Turgor Measurements

2002

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Hyperosmotic stress is known to significantly enhance net uptake of inorganic ions into plant cells. Direct evidence for cell turgor recovery via such a mechanism, however, is still lacking. In the present study, we performed concurrent measurements of net ion fluxes (with the noninvasive microelectrode ion flux estimation technique) and cell turgor changes (with the pressure-probe technique) to provide direct evidence that inorganic ion uptake regulates turgor in osmotically stressed Arabidopsis epidermal root cells. Immediately after onset of hyperosmotic stress (100/100 mm mannitol/sorbitol treatment), the cell turgor dropped from 0.65 to about 0.25 MPa. Turgor recovery started within 2 to 10 min after the treatment and was accompanied by a significant (30-80 nmol m Ϫ2 s Ϫ1 ) increase in uptake of K ϩ , Cl Ϫ , and Na ϩ by root cells. In most cells, almost complete (Ͼ90% of initial values) recovery of the cell turgor was observed within 40 to 50 min after stress onset. In another set of experiments, we combined the voltage-clamp and the microelectrode ion flux estimation techniques to show that this process is, in part, mediated by voltage-gated K ϩ transporters at the cell plasma membrane. The possible physiological significance of these findings is discussed.Improving crop resistance to drought stresses is a long-standing challenge for generations of plant physiologists and agricultural biotechnologists. In the last 15 years, major efforts have been focused on molecular engineering of transgenic species that overexpress genes responsible for biosynthesis of various compatible solutes (Bohnert et al., 1995; Bray, 1997). This approach has been extensively reviewed (Smirnoff, 1998; Bajaj et al., 1999; Bohnert and Shen, 1999; Nuccio et al., 1999;Serrano et al., 1999b; Cushman and Bohnert, 2000). Among the genes targeted were those responsible for biosynthesis of amino acids (Pro, ectoine, and Gly betaine), sugars (Suc, trehalose, and fructan), polyols (mannitol and sorbitol) and quaternary amines (Winicov, 1998; Bajaj et al., 1999; Cushman and Bohnert, 2000; and refs. therein).The practical outcomes of these extensive studies surprisingly are only marginal (Bajaj et al., 1999; Bohnert and Shen, 1999). To our knowledge, there are no reports of any significant improvements in drought tolerance in transgenic crop species in field trials. This is probably due to the complexity of whole-plant responses to water stress. But at the cellular level, are we on the right track in our attempts to improve the plant's ability to withstand water stress?It was traditionally believed that the major function of compatible solutes is osmoregulation (Wyn Jones and Pritchard, 1989; Delauney and Verma, 1993; Bajaj et al., 1999). However, it recently became evident that the functions of compatible solutes are not likely to be as straightforward as initially believed. More and more papers question whether compatible solutes are directly involved in regulation of cell turgor, suggesting instead that their possible regulatory role i...

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“…However, because Pro dehydrogenase is a mitochondrial enzyme (Kiyosue et al, 1996), effective catabolism of Pro would presumably require transport of Pro from the cytosol to the mitochondria. In Arabidopsis NaCl stress or dehydration down-regulates the accumulation of the message for Pro dehydrogenase (Kiyosue et al, 1996;Peng et al, 1996;Verbruggen et al, 1996). Although repression of the synthesis of Pro dehydrogenase could have a role in the long-term regulation of Pro accumulation in response to water stress, the effect of water stress on the activity or stability of Pro dehydrogenase itself has not been determined in Arabidopsis.…”

Section: Pro Accumulation Is Not Correlated With the Tompro1 And Tompmentioning

confidence: 99%

Comparative Analysis of the Regulation of Expression and Structures of Two Evolutionarily Divergent Genes for Δ1-Pyrroline-5-Carboxylate Synthetase from Tomato

Fujita

Maggio

Garcia-Rios³

et al. 1998

Plant Physiology

112

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We isolated two tomato (Lycopersicon esculentum) cDNA clones, tomPRO1 and tomPRO2, specifying ⌬ 1 -pyrroline-5-carboxylate synthetase (P5CS), the first enzyme of proline (Pro) biosynthesis. tomPRO1 is unusual because it resembles prokaryotic polycistronic operons (M.G. García-Ríos, T. Fujita, P.C. LaRosa, R.D. Locy, J.M. Clithero, R.A. Bressan, L.N. Csonka [1997] Proc Natl Acad Sci USA 94: 8249-8254), whereas tomPRO2 encodes a fulllength P5CS. We analyzed the accumulation of Pro and the tomPRO1 and tomPRO2 messages in response to NaCl stress and developmental signals. Treatment with 200 mM NaCl resulted in a >60-fold increase in Pro levels in roots and leaves. However, there was a <3-fold increase in the accumulation of the tomPRO2 message and no detectable induction in the level of the tomPRO1 message in response to NaCl stress. Although pollen contained approximately 100-fold higher levels of Pro than other plant tissues, there was no detectable increase in the level of either message in pollen. We conclude that transcriptional regulation of these genes for P5CS is probably not important for the osmotic or pollenspecific regulation of Pro synthesis in tomato. Using restriction fragment-length polymorphism mapping, we determined the locations of tomPRO1 and tomPRO2 loci in the tomato nuclear genome. Sequence comparison suggested that tomPRO1 is similar to prokaryotic P5CS loci, whereas tomPRO2 is closely related to other eukaryotic P5CS genes.

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Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator.

Cited by 178 publications

References 27 publications

Removal of Feedback Inhibition of Δ1-Pyrroline-5-Carboxylate Synthetase Results in Increased Proline Accumulation and Protection of Plants from Osmotic Stress

Removal of Feedback Inhibition of Δ1-Pyrroline-5-Carboxylate Synthetase Results in Increased Proline Accumulation and Protection of Plants from Osmotic Stress

Turgor Regulation in Osmotically Stressed Arabidopsis Epidermal Root Cells. Direct Support for the Role of Inorganic Ion Uptake as Revealed by Concurrent Flux and Cell Turgor Measurements

Comparative Analysis of the Regulation of Expression and Structures of Two Evolutionarily Divergent Genes for Δ1-Pyrroline-5-Carboxylate Synthetase from Tomato

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