Sulfate transporters in the plant′s response to drought and salinity: Regulation and possible functions

Frontiers in Plant Science

Volumn 5, Issue October, 2014, Pages

  Gallardo, Karine ^a   Courty, Pierre Emmanuel ^b   Le Signor, Christine ^a   Wipf, Daniel ^c   Vernoud, Vanessa ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

Abiotic stresses; Arabidopsis; M. truncatula; Sulfate; Transporters

Indexed keywords

EID: 84908371552     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00580     Document Type: Review

References (55)

1. Allen, J. W., and Shachar-Hill, Y. (2009). Sulfur transfer through an arbuscular mycorrhiza. PlantPhysiol. 149, 549-560. doi: 10.1104/pp.108.129866
2. Arraouadi, S., Badri, M., Abdelly, C., Huguet, T., and Aouani, M. E. (2012). QTL mapping of physiological traits associated with salt tolerance in Med-icago truncatula Recombinant Inbred Lines. Genomics 99, 118-125. doi: 10.1016/j.ygeno.2011.11.005
3. Augé, R. M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3-42. doi: 10.1007/s005720100097
4. Awazuhara, M., Fujiwara, T., Hayashi, H., Watanabe-Takahashi, A., Takahashi, H., and Saito, K. (2005). The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Plant Physiol. 125, 95-105. doi: 10.1111/j.1399-3054.2005.00543.x
5. Barberon, M., Berthomieu, P., Clairotte, M., Shibagaki, N., Davidian, J.-C., and Gosti, F. (2008). Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol. 180, 608-619. doi: 10.1111/j.1469-8137.2008. 02604.x
6. Bordat, A., Savois, V., Nicolas, M., Salse, J., Chauveau, A., Bourgeois, M., etal. (2011). Translational genomics in legumes allowed placingin silico 5460 unigenes on the pea functional map and identified candidate genes in Pisum sativum L. G3 (Bethesda) 1, 93-103. doi: 10.1534/g3.111.000349
7. Buchner, P., Takahashi, H., and Hawkesford, M. J. (2004). Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55, 1765-1773. doi: 10.1093/jxb/erh206
8. Cao, M. J., Wang, Z., Wirtz, M., Hell, R., Oliver, D. J., and Xiang, C. B. (2013). SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. PlantJ. 73, 607-616. doi: 10.1111/tpj.12059
9. Cao, M. J., Wang, Z., Zhao, Q., Mao, J. L., Speiser, A., Wirtz, M., etal. (2014). Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J. 77, 604-615. doi: 10.1111/tpj. 12407
10. Casieri, L., Ait Lahmidi, N., Doidy, J., Veneault-Fourrey, C., Migeon, A., Bonneau, L., et al. (2013). Biotrophic transportome in mutualistic plant-fungal interactions. Mycorrhiza 23, 597-625. doi: 10.1007/s00572-013-0496-9
11. Casieri, L., Gallardo, K., and Wipf, D. (2012). Transcriptional response of Med-icago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235, 1431-1447. doi: 10.1007/s00425-012-1645-7
12. Chan, K. X., Wirtz, M., Phua, S. Y., Estavillo, G. M., and Pogson, B. J. (2013). Balancing metabolites in drought: the sulfur assimilation conundrum. Trends PlantSci. 18, 18-29. doi: 10.1016/j.tplants.2012.07.005
13. Dalmais, M., Schmidt, J., Le Signor, C., Moussy, F., Burstin, J., Savois, V., et al. (2008). UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol. 9, R43. doi: 10.1186/gb-2008-9-2-r43
14. Deulvot, C., Charrel, H., Marty, A., Jacquin, F., Donnadieu, C., Lejeune-Henaut, I., et al. (2010). Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genomics 11:468. doi: 10.1186/14712164-11-468
15. Ding, D., Zhang, L., Wang, H., Liu, Z., Zhang, Z., and Zheng, Y. (2009). Differential expression of miRNAs in response to salt stress in maize roots. Ann. Bot. 103, 29-38. doi: 10.1093/aob/mcn205
16. El-Soda, M., Kruijer, W., Malosetti, M., Koornneef, M., and Aarts, M. G. (2014). Quantitative trait loci and candidate genes underlying genotype by environment interaction in the response of Arabidopsis thaliana to drought. PlantCell Environ. doi: 10.1111/pce.12418 [Epub ahead of print].
17. Ernst, L., Goodger, J. Q., Alvarez, S., Marsh, E. L., Berla, B., Lockhart, E., et al. (2010). Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. J. Exp. Bot. 61, 3395-3405. doi: 10.1093/jxb/erq160
18. Friesen, M. L., Cordeiro, M. A., Penmetsa, R. V., Badri, M., Huguet, T., Aouani, M. E., et al. (2010). Population genomic analysis ofTunisian Medicago truncatula reveals candidates for local adaptation. PlantJ. 63, 623-635. doi: 10.1111/j.1365-313X.2010.04267.x
19. Frugoli, J., and Harris, J. (2001). Medicago truncatula on the move! Plant Cell. 13, 458-463. doi: 10.1105/tpc.13.3.458
20. Geng, Y., Wu, R., Wee, C. W., Xie, F., Wei, X., Chan, P. M., et al. (2013). A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. PlantCell 25,2132-2154. doi: 10.1105/tpc.113.112896
21. Giovannetti, M., Tolosano, M., Volpe, V., Kopriva, S., and Bonfante, P. (2014). Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotusjaponicus. New Phytol. 204, 609-619. doi: 10.1111/nph.12949
22. Goodger, J. Q., and Schachtman, D. P. (2010). Re-examining the role of ABA as the primary long-distance signal produced by water-stressed roots. Plant Signal. Behav. 5, 1298-1301. doi: 10.4161/psb.5.10.13101
23. Gray, L. E., and Gerdemann, J. W. (1973). Uptake of sulphur-35 by vesicular-arbuscular mycorrhizae. PlantSoil 39, 687-689. doi: 10.1007/BF00264184
24. Ha, C. V., Leyva-Gonzalez, M. A., Osakabe, Y., Tran, U. T., Nishiyama, R., Watanabe, Y., etal. (2014). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111, 851-856. doi: 10.1073/pnas.1322135111
25. Huang, D., Wu, W., Abrams, S. R., and Cutler, A. J. (2008). The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J. Exp. Bot. 59, 2991-3007. doi: 10.1093/jxb/ern155
26. Hyung, D., Lee, C., Kim, J. H., Yoo, D., Seo, Y. S., Jeong, S. C., et al. (2014). Cross-family translational genomics of abiotic stress-responsive genes between Arabidopsis and Medicago truncatula. PLoS ONE 9:e91721. doi: 10.1371/jour-nal.pone.0091721
27. Juenger, T. E., McKay, J. K., Hausmann, N., Keurentjes, J. J. B., Sen, S., Stowe, K. A., et al. (2005). Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: Delta C-13, stomatal conductance and transpiration efficiency. Plant Cell Environ. 28, 697-708. doi: 10.1111/j.1365-3040.2004.01313.x
28. Kataoka, T., Hayashi, N., Yamaya, T., and Takahashi, H. (2004a). Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol. 136, 4198-4204. doi: 10.1104/pp.104.045625
29. Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., etal. (2004b). Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16, 2693-2704. doi: 10.1105/tpc.104.023960
30. Kawashima, C. G., Matthewman, C. A., Huang, S., Lee, B. R., Yoshimoto, N., Koprivova, A., etal. (2011). Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863-876. doi: 10.1111/j.1365-313X.2011.04547.x
31. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., et al. (2007). The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363. doi: 10.1111/j.1365-313X.2007.03052.x
32. Krusell, L., Krause, K., Ott, T., Desbrosses, G., Kramer, U., Sato, S., etal. (2005). The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. PlantCell 17, 1625-1636. doi: 10.1105/tpc.104. 030106
33. Kumar, S., Asif, M. H., Chakrabarty, D., Tripathi, R. D., and Trivedi, P. K. (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. doi: 10.1007/s10142-010-0207-y
34. Le Signor, C., Savois, V., Aubert, G., Verdier, J., Nicolas, M., Pagny, G., etal. (2009). Optimizing TILLING populations for reverse genetics in Medicago truncatula. Plant Biotechnol. J. 7, 430-441. doi: 10.1111/j.1467-7652.2009.00410.x
35. Li, D., Su, Z., Dong, J., and Wang, T. (2009). An expression database for roots of the model legume Medicago truncatula under salt stress. BMC Genomics 10:517. doi: 10.1186/1471-2164-10-517
36. McKay, J. K., Richards, J. H., Nemali, K. S., Sen, S., Mitchell-Olds, T., Boles, S., et al. (2008). Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, Kas-1 x Tsu-1. Evolution 62, 3014-3026. doi: 10.1111/j.1558-5646.2008.00474.x
37. Nishiyama, R., Le, D. T., Watanabe, Y., Matsui, A., Tanaka, M., Seki, M., et al. (2012). Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE 7:e32124. doi: 10.1371/journal.pone.0032124
38. Pandey, N., Ranjan, A., Pant, P., Tripathi, R. K., Ateek, F., Pandey, H. P., et al. (2013). CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216. doi: 10.1186/1471-2164-14-216
39. Perera, I. Y., Hung, C. Y., Moore, C. D., Stevenson-Paulik, J., and Boss, W. F. (2008). Transgenic Arabidopsis plants expressing the type 1 inositol 5-phosphatase exhibit increased drought tolerance and altered abscisic acid signaling. Plant Cell 20, 2876-2893. doi: 10.1105/tpc.108.061374
40. Rhodes, L. H., and Gerdemann, J. W. (1978a). Hyphal translocation and uptake of sulfur by vesicular-arbuscular mycorrhizae of onion. Soil Biol. Biochem. 10, 355-360. doi: 10.1016/0038-0717(78)90057-3
41. Rhodes, L. H., and Gerdemann, J. W. (1978b). Influence of phosphorus nutrition on sulphur uptake by vesicular arbuscular. Soil Biol. Biochem. 10, 361-364. doi: 10.1016/0038-0717(78)90058-5
42. Roux, B., Rodde, N., Jardinaud, M. F., Timmers, T., Sauviac, L., Cottret, L., etal. (2014). An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. PlantJ. 77, 817-837. doi: 10.1111/tpj.12442
43. Sieh, D., Watanabe, M., Devers, E. A., Brueckner, F., Hoefgen, R., and Krajinski, F. (2013). The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytol. 197, 606-616. doi: 10.1111/nph.12034
44. Takahashi, H., Watanabe-Takahashi, A., Smith, F. W., Blake-Kalff, M., Hawkesford, M. J., and Saito, K. (2000). The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23, 171-182. doi: 10.1046/j.1365-313x.2000.00768.x
45. Vaiin, S., Cliquet, J. B., Personeni, E., Avice, J.-C., and Lemauviel-Lavenant, S. (2010). How does sulphur availability modify N acquisition of white clover (Trifolium repens L.).? J. Exp. Bot. 61, 225-234. doi: 10.1093/jxb/erp303
46. Wang, Y., Yang, L., Zheng, Z., Grumet, R., Loescher, W., Zhu, J. K., et al. (2013). Tran-scriptomic and physiological variations of three Arabidopsis ecotypes in response to salt stress. PLoS ONE 8:e69036. doi: 10.1371/journal.pone.0069036
47. Wilkinson, S., and Davies, W. J. (2002). ABA-based chemical signaling: the coordination of responses to stress in plants. Plant Cell Environ. 25, 195-210. doi: 10.1046/j.0016-8025.2001.00824.x
48. Xiong, L., Ishitani, M., Lee, H., and Zhu, J. K. (2001). The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress-and osmotic stress-responsive gene expression. Plant Cell 13, 2063-2083. doi: 10.1105/tpc.13.9.2063
49. Yoshimoto, N., Inoue, E., Saito, K., Yamaya, T., and Takahashi, H. (2003). Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol. 131, 1511-1517. doi: 10.1104/pp.014712
50. Yoshimoto, N., Inoue, E., Watanabe-Takahashi, A., Saito, K., and Takahashi, H. (2007). Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol. 145, 378-388. doi: 10.1104/pp.107.105742
51. Zhang, J. Y., Cruz, D. E., Carvalho, M. H., Torres-Jerez, I., Kang, Y., Allen, S. N., et al. (2014a). Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant Cell Environ. In press (free access online). doi: 10.1111/pce.12328 [Epub ahead of print].
52. Zhang, B., Pasini, R., Dan, H., Joshi, N., Zhao, Y., Leustek, T., etal. (2014b). Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. PlantJ. 77, 185-197. doi: 10.1111/tpj.12376
53. Zhang, X., Lu, G., Long, W., Zou, X., Li, F., and Nishio, T. (2014c). Recent progress in drought and salt tolerance studies in Brassica crops. Breed Sci. 64, 60-73. doi: 10.1270/jsbbs.64.60
54. Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., and Luo, L. (2010). Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J. Exp. Bot. 61,4157-4168. doi: 10.1093/jxb/erq237
55. Zuber, H., Davidian, J.-C., Aubert, G., Aime, D., Belghazi, M., Lugan, R., et al. (2010). The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. PlantPhysiol. 154, 913-926. doi: 10.1104/pp.110.162123