Unraveling the role of urea hydrolysis in salt stress response during seed germination and seedling growth in Arabidopsis thaliana
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eLife assessment
This important study advances our understanding of the molecular mechanism underlying salt stress-induced inhibition of seed germination and seedling growth. The evidence supporting the conclusions is convincing, with rigorous genetic, physiological, and metabolic analyses. This paper will be of interest to plant stress biologists and crop breeders.
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Abstract
Urea is intensively utilized as a nitrogen fertilizer in agriculture, originating either from root uptake or from catabolism of arginine by arginase. Despite its extensive use, the underlying physiological mechanisms of urea, particularly its adverse effects on seed germination and seedling growth under salt stress, remain unclear. In this study, we demonstrate that salt stress induces excessive hydrolysis of arginine-derived urea, leading to an increase in cytoplasmic pH within seed radical cells, which, in turn, triggers salt-induced inhibition of seed germination (SISG) and hampers seedling growth. Our findings challenge the long-held belief that ammonium accumulation and toxicity are the primary causes of SISG, offering a novel perspective on the mechanism underlying these processes. This study provides significant insights into the physiological impact of urea hydrolysis under salt stress, contributing to a better understanding of SISG.
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eLife assessment
This important study advances our understanding of the molecular mechanism underlying salt stress-induced inhibition of seed germination and seedling growth. The evidence supporting the conclusions is convincing, with rigorous genetic, physiological, and metabolic analyses. This paper will be of interest to plant stress biologists and crop breeders.
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Reviewer #1 (Public Review):
Salt-inhibited germination and growth in Arabidopsis and other plant species. Here the authors demonstrated that part of that inhibitory effect is caused by the arginine-derived urea hydrolysis, a novel mechanism. They also postulated that urea transport is involved in germination inhibition, but they do not link urea transport from cotyledons to pH changes in roots. At last, they generalized the mechanisms to other glycophytic crops and halophytic plants, but the salt concentration used is the same for the four groups, which are supposed to have very different salt tolerance ranges, questioning the validity of this generalization.
Overall, the authors have provided well-organized genetic and pharmacological evidence to support most of their conclusions. -
Reviewer #2 (Public Review):
Urea is widely utilized in agriculture. In this study, the authors the mechanism underlying the adverse impact of urea on seed germination and seedling growth under salt stress conditions. The results show that salt stress induces a pronounced hydrolysis of urea, resulting in an elevation of cytoplasmic pH and subsequent inhibition of seed germination. These findings challenge the previous notion that ammonium accumulation is the primary cause of salt-induced inhibition of germination, thereby offering novel insights into this process.
The authors have provided well-organized genetic or biochemical evidence to support most of their conclusions.
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Reviewer #3 (Public Review):
This work submitted by Bu et al. investigated mechanisms of how salt stress-induced arginine catabolism, which is catalyzed by arginase and urease, inhibits seed germination and seedling growth in Arabidopsis using a combination of genetic, biochemical, and live-cell imaging approaches. Their results showed that the two steps for the turnover of arginine into ammonia and the transport of urea from the cotyledon to the root are required for the salt-induced inhibition of seed germination (SISG). Further analysis showed that the cellular accumulation of the end product ammonia is not associated with SISG, but it is the cytoplasmic alkaline stress that primarily causes SISG. Interestingly, they found that the mechanism underlying SISG is conserved in other plant species. In general, this work will be valuable …
Reviewer #3 (Public Review):
This work submitted by Bu et al. investigated mechanisms of how salt stress-induced arginine catabolism, which is catalyzed by arginase and urease, inhibits seed germination and seedling growth in Arabidopsis using a combination of genetic, biochemical, and live-cell imaging approaches. Their results showed that the two steps for the turnover of arginine into ammonia and the transport of urea from the cotyledon to the root are required for the salt-induced inhibition of seed germination (SISG). Further analysis showed that the cellular accumulation of the end product ammonia is not associated with SISG, but it is the cytoplasmic alkaline stress that primarily causes SISG. Interestingly, they found that the mechanism underlying SISG is conserved in other plant species. In general, this work will be valuable for plant biologists to deeply dissect the complex mechanism that controls salt stress-induced inhibition of plant growth and development in the future.
The conclusions derived from this work are well supported by the data, but some aspects of data analysis need to be clarified and extended.
(1) Inhibition of arginine hydrolysis by enzyme inhibitors (NOHA for arginase and PPD for urease) significantly improved seed germination and seedling growth (Figure 2). It seems that the suppressive effect of NOHA against the salt-induced inhibition of seedling growth is dose-dependent (Figure 2b). Whether NOHA effect on SISG is also dose-dependent and application of a certain level of NOHA can fully rescue the phenotype of SISG remains to be answered. The answers may help to explain the genetic data shown in Figure 3c, where either single (argah1 and argah2) or double (argah1/argah2) mutants partially rescued the phenotype of SISG. However, arginase activity, particularly in argah1 and argah2, is not closely correlated to the phenotype shown in Figure 3c and 3d.
(2) The data shown in Figure 4b and 4e were not fully consistent. The percentage of seed germination rate was about 70% when treated with the highest concentration (7.5 μM) of PPD, but was less than 40% for the aturease mutant.
(3) Cellular pH values detected at the seed germination stage were not convincing. In the text, they did not describe the results showing that the cytoplasmic pH values in hypocotyl and cotyledon cells were alkaline and not affected by NaCl treatment, and PPD treatment only restored the alkaline cytoplasmic pH to that of the control (Figure 7b). This raises two questions: is it true that cytoplasmic pH values are different between root and cotyledon/hypocotyl cells under normal growth conditions? and does PPD treatment alter the cytoplasmic pH only in roots?
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