Abstract
Arsenic (As) contamination of rice grains affects millions of people worldwide. In this study, we found that sulfur application (20As+120S) decreased As concentration in rice grains by 44 % compared to grains without sulfur application (20As+0S). Importantly, sulfur application decreased arsenate [As(V)] and arsenite [As(III)] concentration in rice grains significantly, while there was no significant effect on dimethylarsenate (DMA) concentration. To elucidate the molecular basis of As accumulation in rice grains, we performed Illumina sequencing to acquire the differentially expressed genes induced by arsenate and sulfur treatments. By contrast with the control, the expression of 1,000 genes was found to be changed significantly, with 46 genes up-regulated and 954 genes down-regulated in grains grown in arsenate-contaminated soil (20As+0S). Between samples of control and arsenate together with sulfur treatment (20As+120S), 1,169 genes expressed significantly differently, with 16 genes up-regulated and 1,153 genes down-regulated. Sulfur application significantly changed the expression of genes involved in As metabolism in rice grains, significantly down-regulated phosphate transporter gene OsPT23 and aquaporin gene OsTIP4;2, while ABC transporter genes (OsABCG5, OsABCI7_2 and OsABC6) and phytochelatin synthase genes (OsPCS1, OsPCS3 and OsPCS13) were up-regulated. These results provide an insight into the molecular basis of how sulfur assimilation regulates As accumulation in rice grains.
Similar content being viewed by others
Abbreviations
- As:
-
Arsenic
- As(III):
-
Arsenite
- As(V):
-
Arsenate
- ABC superfamily:
-
ATP-binding cassette superfamily
- ABCA:
-
ABC subfamily A
- ABCB:
-
ABC subfamily B
- ABCC:
-
ABC subfamily C
- ABCD:
-
ABC subfamily D
- ABCF:
-
ABC subfamily F
- ABCG:
-
ABC subfamily G
- ABCI:
-
ABC subfamily I
- ATPS:
-
ATP sulfurylase
- AR:
-
Arsenate reductase
- DGE:
-
Digital gene expression
- DEGs:
-
Differentially expressed genes
- DMA:
-
Dimethylarsenate
- γ–ECS:
-
γ-Glutamylcysteinesynthetase
- GSH:
-
Glutathione
- GS:
-
Glutathione synthetase
- GST:
-
Glutathione S-transferase
- MMA:
-
Monomethylarsenate
- OAS-TL:
-
O-Acetylserine (thiol) lyase
- PCs:
-
Phytochelatins
- PCS:
-
Phytochelatin synthases
- PT:
-
Phosphate transporter
- PIPs:
-
Plasma membrane intrinsic proteins
- TIPs:
-
Tonoplast intrinsic proteins
- NIPs:
-
Nodulin 26-like intrinsic membrane proteins
- SIPs:
-
Small and basic intrinsic proteins
- qRT-PCR:
-
Quantitative RT-PCR
- S:
-
Sulfur
- SAT:
-
Serine acetyltransferase
- SiR:
-
Sulfite reductase
- TMAs:
-
Trimethylarsine
References
Bleeker PM, Hakvoort HWJ, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerance Holcus lanatus. Plant J 45:917–929
Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, Kumar S, Rai A, Pandey A, Nigam D, Tripathi RD, Tuli R (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702
Chen Y, Moore KL, Miller AJ, McGrath SP, Ma JF, Zhao FJ (2015) The role of nodes in arsenic storage and distribution in rice. J Exp Bot 66(13):3717–3724
Clemens S, Kim E, Neumann D, Schroeder J (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333
Dixit G, Singh AP, Kumar A, Singh PK, Kumar S, Dwived S, Trivedi PK, Pandey V, Norton GJ, Dhankher OP, Tripathi RD (2015) Sulfur mediated reduction of arsenic toxicity involves efficient thiol metabolism and the antioxidant defense system in rice. J Hazard Mater 298:241–251
Duan GL, Kamiya T, Ishikawa S, Arao T, Fujiwara T (2012) Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell Physiol 53:154–163
Duan GL, Liu WJ, Chen XP, Hu Y, Zhu YG (2013) Association of arsenic with nutrient elements in rice plants. Metallomics 5:784–792
Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag S, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genomics 11:648–667
El-Zohri M, Odjegba V, Ma L, Rathinasabapathi B (2015) Sulfate influx transporters in Arabidopsis thaliana are not involved in arsenate uptake but critical for tissue nutrient status and arsenate tolerance. Planta 241(5):1109–1118
Fan J, Xia X, Hu Z, Ziadi N, Liu C (2013) Excessive sulfur supply reduces arsenic accumulation in brown rice. Plant Soil Environ 59:169–174
Heiss S, Wachter A, Bogs J, Cobbett C, Rausch T (2003) Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure. J Exp Bot 54:1833–1839
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot. doi:10.1093/jxb/erv063
Hu ZY, Zhu YG, Li M, Zhang LG, Cao ZH, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393
Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Trivedi PK (2011) Differential expression and alternative splicing of rice sulphate transporter family members regulate sulphur status during plant growth, development and stress conditions. Funct Integr Genomics 11:259–273
Liu F1, Chang XJ, Ye Y, Xie WB, Wu P, Lian XM (2011) Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Plant Physiol 152:2211–2221
Liu Q, Guo Y, Li J, Long J, Zhang B, Shyr Y (2012) Steps to ensure accuracy in genotype and SNP calling from Illumina sequencing data. BMC Genomics13 Suppl 8:S8. doi: 10.1186/1471-2164-13-S8-S8
Lombi E, Schechel KG, Pallon AM, Pallon J, Carey YG, Zhu YG, Meharg AA (2009) Speciation and distribution of arsenic and location of nutrients in rice grains. New Phytol 184:193–201
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43
Meharg AA, Macnair MR (1992) Suppression of the high-affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524
Norton GJ, Lou-Hing DE, Meharg AA, Price AH (2008) Rice-arsenate interactions in hydroponics: whole genome transcriptional analysis. J Exp Bot 59:2267–2276
Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113–1122
Raab A, Schat H, Meharg AA, Feldmann J (2005) Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic–phytochelatin complexes during exposure to high arsenic concentrations. New Phytol 168:551–558
Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Expr Bot 71:89–98
Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642
Song WY, Park J, Mendoza-Cózatl DG, Suter-Grotemeyer M, Shim D, Hörtensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroeder JI, Lee YS, Martinoia E (2010) Arsenic tolerance in Arabidopsisis mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107:21187–21192
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (L.f) Royle. Environ Sci Technol 41:2930–2936
Srivastava AK, Srivastava S, Mishra S, Suprasanna P, D’Souza SF (2014) Identification of redox-regulated components of arsenate (AsV) tolerance through thiourea supplementation in rice. Metallomics 6:1718–1730
Su YH, McGrath SP, Zhu YG, Zhao FJ (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 108:434–441
Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol 159:1571–1581
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372
Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata: uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561
Wang LH, Duan GL, Williams PN, Zhu YG (2008) Influences of phosphorus starvation on OsACR2.1 expression and arsenic metabolism in rice seedlings. Plant Soil 313:129–139
Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldmann J, Meharg AA (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859
Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599
Yu LJ, Luo YF, Liao B, Xie LJ, Chen L, Xiao S, Li JT, Hu SN, Shu WS (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol 195:97–112
Zhang J, Zhao QZ, Duan GL, Huang YC (2011) Influence of sulphur on arsenic accumulation and metabolism in rice seedlings. Environ Exp Bot 72:34–40
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559
Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A, Meharg AA, Williams PN (2008) High percentage inorganic arsenic content of mining impacted and non-impacted Chinese rice. Environ Sci Technol 42:5008–5013
Acknowledgments
This work was supported by the National Natural Science Foundation of China (41103062 and 41371458) and the Innovation Scientists and Technicians Troop Construction Projects of Henan Province (94200510003).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Zhang, J., Zhao, CY., Liu, J. et al. Influence of Sulfur on Transcription of Genes Involved in Arsenic Accumulation in Rice Grains. Plant Mol Biol Rep 34, 556–565 (2016). https://doi.org/10.1007/s11105-015-0937-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-015-0937-z