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Sulfate influx transporters in Arabidopsis thaliana are not involved in arsenate uptake but critical for tissue nutrient status and arsenate tolerance

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Abstract

Main conclusion

Arsenic, a non-nutrient metalloid is toxic to plants but many details on the physiology of plant adaptation to arsenic stress are not well understood. This work provides new insights about the role of sulfur assimilation in arsenate uptake, growth and arsenic tolerance. Research reported here indicates that two high affinity sulfate transporters in Arabidopsis thaliana are not involved in root uptake of arsenate. Further this study revealed that sulfate status influenced thiol levels, elemental nutrients, growth and arsenate tolerance.

The hypothesis that arsenate may be transported via sulfate transporters, SULTR1;1 and SULTR1;2 in Arabidopsis, was tested. The double mutant of sultr1;1 sultr1;2 exhibited significantly less growth than the wild-type or the single mutants. The double mutant’s sulfur content was significantly lower than the wild-type but the single mutants were similar to the wild-type confirming the redundant functions of SULTR1;1 and SULTR1;2. Gene expression analyses indicated that the double mutant’s sulfate uptake could be explained by the expressions of SULTR1;3, SULTR2;1, and SULTR2;2 in its roots. Following arsenate supply to the roots, the double mutant accumulated significantly less arsenic in the roots and the shoots than did the single mutants and the wild-type. The double mutant accumulated significantly less potassium and phosphorus also. 35S sulfate supplied to wild-type or double mutant roots showed that sulfate uptake was not inhibited by arsenate. Taken together, these results indicate that root uptake of arsenate is probably not via sulfate transporters, but the poor growth of the double mutant of sultr1;1 and sultr1;2 was due to its poor sulfate status and decreased levels of thiols, which had pleiotropic effects on the root uptake and translocation of potassium and phosphorus and arsenic tolerance.

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Abbreviations

As(V):

Arsenate

As(III):

Arsenite

DTNB:

5,5’ Dithiobis (2-nitrobenzoic acid)

ICP-AES:

Inductively coupled plasma atomic emission spectrometry

ICP-MS:

Inductively coupled plasma mass spectrometry

RT-PCR:

Reverse transcription-polymerase chain reaction

SULTR:

sulfate transporter

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Acknowledgments

The authors sincerely appreciate the support of the Fulbright organization for the Scholar Program Fellowship awarded to Manal El-Zohri and Victor Odjegba (G-68434198). They thank Dr. Francoise Gosti of the Institute National de la Recherché Agronomique (Universite Montpellier II, France) for providing the seeds of sulfate transporter mutants and Mr. Evandro da Silva (University of Florida) for help with the operation of ICP-MS.

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Correspondence to Bala Rathinasabapathi.

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El-Zohri, M., Odjegba, V., Ma, L. et al. Sulfate influx transporters in Arabidopsis thaliana are not involved in arsenate uptake but critical for tissue nutrient status and arsenate tolerance. Planta 241, 1109–1118 (2015). https://doi.org/10.1007/s00425-015-2241-4

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