Comparative transcriptome analysis of the metal hyperaccumulator Noccaea caerulescens

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Halimaa, Pauliina ^a   Blande, Daniel ^a   Aarts, Mark G M ^b   Tuomainen, Marjo ^a   Tervahauta, Arja ^a   Kärenlampi, Sirpa ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Brassicaceae; Deep sequencing; Hyperaccumulation; Metal tolerance; NGS; Noccaea caerulescens; RNA Seq; Thlaspi caerulescens

Indexed keywords

EID: 84902270568     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00213     Document Type: Review

References (56)

1. Aina, R., Sgorbati, S., Santagostino, A., Labra, M., Ghiani, A., and Citterio, S. (2004). Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol. Plantarum 121, 472-480. doi: 10.1111/j.1399-3054.2004.00343.x
2. Assunção, A. G. L., Ten Bookum, W. M., Nelissen, H. J. M., Vooijs, R., Schat, H., and Ernst, W. H. O. (2003a). A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol. 159, 383-390. doi: 10.1046/j.1469-8137.2003.00758.x
3. Assunção, A. G. L., Schat, H., and Aarts, M. G. M. (2003b). Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol. 159, 351-360. doi: 10.1046/j.1469-8137.2003.00820.x
4. Assunção, A. G. L., Ten Bookum, W. M., Nelissen, H. J. M., Vooijs, R., Schat, H., and Ernst, W. H. O. (2003c). Differential metal tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol. 159, 411-419. doi: 10.1046/j.1469-8137.2003.00819.x
5. Assunção, A. G. L., Pieper, B., Vromans, J., Lindhout, P., Aarts, M. G. M., and Schat, H. (2006). Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol.170, 21-32. doi: 10.1111/j.1469-8137.2005.01631.x
6. Barrera-Figueroa, B. E., Gao, L., Wu, Z., Zhou, X., Zhu, J., Jin, H., et al. (2012). High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol. 12:132. doi: 10.1186/1471-2229-12-132
7. Beitz, E. (2000). TEXtopo: shaded membrane protein topology plots in LATEX 2ε. Bioinformatics 16, 1050-1051. doi: 10.1093/bioinformatics/16.11.1050
8. Bernard, C., Roosens, N., Czernic, P., Lebrun, M., and Verbruggen, N. (2004). A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett. 569, 140-148. doi: 10.1016/j.febslet.2004.05.036
9. Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., and Lux, A. (2007). Zinc in plants. New Phytol. 173, 677-702. doi: 10.1111/j.1469-8137.2007.01996.x
10. Chen, L., Wang, T., Zhao, M., Tian, Q., and Zhang, W. H. (2012). Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235, 375-386. doi: 10.1007/s00425-011-1514-9
11. Choi, C. S., and Sano, H. (2007). Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol. Genet. Genomics 277, 589-600. doi: 10.1007/s00438-007-0209-1
12. Cosio, C., Martinoia, E., and Keller, C. (2004). Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens andArabidopsis halleri at the leaf cellular level. Plant Physiol. 134, 716-725. doi: 10.1104/pp.103.031948
13. Craciun, A. R., Meyer, C.-L., Chen, J., Roosens, N., De Groodt, R., Hilson, P., et al. (2012). Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation. J. Exp. Bot. 63, 4179-4189. doi: 10.1093/jxb/ers104
14. Deniau, A. X., Pieper, B., Ten Bookum, W. M., Lindhout, P., Aarts, M. G. M., and Schat, H. (2006). QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor. Appl. Genet.113, 907-920. doi: 10.1007/s00122-006-0350-y
15. Derrien, T., Estellé, J., Sola, S. M., Knowles, D. G., Raineri, E., Guigó, R., et al. (2012). Fast computation and applications of genome mappability. PLoS ONE 7:e30377. doi: 10.1371/journal.pone.0030377
16. Dillies, M.-A., Rau, A., Aubert, J., Hennequet-Antier, C., Jeanmougin, M., Servant, N., et al. (2012). A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform. 14, 671-683. doi: 10.1093/bib/bbs046
17. Eide, D., Broderius, M., Fett, J., and Guerinot, M. L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. U.S.A. 93, 5624-5628. doi: 10.1073/pnas.93.11.5624
18. Escarré, J., Lefèbvre, C., Frérot, H., Mahieu, S., and Noret, N. (2013). Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media. Plant Soil 370, 197-221. doi: 10.1007/s11104-013-1618-z
19. Freeman, J. L., Garcia, D., Kim, D., Hopf, A., and Salt, D. E. (2005). Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol. 137, 1082-1091. doi: 10.1104/pp.104.055293
20. Grossoehme, N. E., Akilesh, S., Guerinot, M. L., and Wilcox, D. E. (2006). Metal-binding thermodynamics of the histidine-rich sequence from the metal-transport protein IRT1 of Arabidopsis thaliana. Inorg. Chem. 45, 8500-8508. doi: 10.1021/ic0606431
21. Halimaa, P., Lin, Y.-F., Ahonen, V., Blande, D., Clemens, S., Gyenesei, A., et al. (2014). Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ. Sci. Technol. 48, 3344-3353. doi: 10.1021/es4042995
22. Hammond, J. P., Bowen, H. C., White, P. J., Mills, V., Pyke, K. A., Baker, A. J. M., et al. (2006). A comparison of theThlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol. 170, 239-260. doi: 10.1111/j.1469-8137.2006.01662.x
23. Hanikenne, M., Talke, I. N., Haydon, M. J., Lanz, C., Nolte, A., Motte, P., et al. (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391-395. doi: 10.1038/nature06877
24. Kerkeb, L., Mukherjee, I., Chatterjee, I., Lahner, B., Salt, D. E., and Connolly, E. L. (2008). Iron-induced turnover of the Arabidopsis Iron-Regulated Transporter1 metal transporter requires lysine residues. Plant Physiol. 146, 1964-1973. doi: 10.1104/pp.107.113282
25. Koch, M. A., and German, D. A. (2013). Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Front. Plant Sci. 4:267. doi: 10.3389/fpls.2013.00267
26. Korshunova, Y., Eide, D., Clark, G., Guerinot, M., and Pakrasi, H. (1999). The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40, 37-44. doi: 10.1023/A:1026438615520
27. Lochlainn, S. Ó., Bowen, H. C., Fray, R. G., Hammond, J. P., King, G. J., White, P. J., et al. (2011). Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS ONE6:e17814. doi: 10.1371/journal.pone.0017814
28. Lombi, E., Zhao, F. J., Dunham, S. J., and McGrath, S. P. (2000). Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol. 145, 11-20. doi: 10.1046/j.1469-8137.2000.00560.x
29. Marquès, L., Cossegal, M., Bodin, S., Czernic, P., and Lebrun, M. (2004). Heavy metal specificity of cellular tolerance in two hyperaccumulating plants, Arabidopsis halleri and Thlaspi caerulescens. New Phytol. 164, 289-295. doi: 10.1111/j.1469-8137.2004.01178.x
30. Meerts, P., and Van Isacker, N. (1997). Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol. 133, 221-231. doi: 10.1023/A:1009717619579
31. Monsant, A. C., Kappen, P., Wang, Y., Pigram, P. J., Baker, A. J. M., and Tang, C. (2011). In vivo speciation of zinc inNoccaea caerulescens in response to nitrogen form and zinc exposure. Plant Soil 348, 167-183. doi: 10.1007/s11104-011-0887-7
32. Ou, X., Zhang, Y., Xu, C., Lin, X., Zang, Q., Zhuang, T., et al. (2012). Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE7:e41143. doi: 10.1371/journal.pone.0041143
33. Peer, W. A., Mamoudian, M., Lahner, B., Reeves, R. D., Murphy, A. S., and Salt, D. E. (2003). Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol. 159, 421-430. doi: 10.1046/j.1469-8137.2003.00822.x
34. Potocki, S., Valensin, D., Camponeschi, F., and Kozlowski, H. (2013). The extracellular loop of IRT1 ZIP protein-the chosen one for zinc? J. Inorg. Biochem. 127, 246-252. doi: 10.1016/j.jinorgbio.2013.05.003
35. Rapaport, F., Khanin, R., Liang, Y., Krek, A., Zumbo, P., Mason, C. E., et al. (2013). Comprehensive evaluation of differential expression analysis methods for RNA-seq data. Genome Biol. 14:R95. doi: 10.1186/gb-2013-14-9-r95
36. Rascio, N., and Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci. 180, 169-181. doi: 10.1016/j.plantsci.2010.08.016
37. Reeves, R. D., Schwartz, C., Morel, J. L., and Edmondson, J. (2001). Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int. J. Phytoremediat. 3, 145-172. doi: 10.1080/15226510108500054
38. Richau, K. H., and Schat, H. (2009). Intraspecific variation of nickeland zinc accumulation and tolerance in the hyperaccumulatoro Thlaspi caerulescens. Plant Soil 314, 253-262. doi: 10.1007/s11104-008-9724-z
39. Rigola, D., Fiers, M., Vurro, E., and Aarts, M. G. M. (2006). The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis. New Phytol. 170, 753-765. doi: 10.1111/j.1469-8137.2006.01714.x
40. Robinson, B. H., Leblanc, M., Petit, D., Brooks, R. R., Kirkman, J. H., and Gregg, P. E. H. (1998). The potential ofThlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203, 47-56. doi: 10.1023/A:1004328816645
41. Rogers, E. E., Eide, D. J., and Guerinot, M. L. (2000). Altered selectivity in an Arabidopsis metal transporter. Proc. Natl. Acad. Sci. U.S.A. 97, 12356-12360. doi: 10.1073/pnas.210214197
42. Romero, I. G., Ruvinsky, I., and Gilad, Y. (2012). Comparative studies of gene expression and the evolution of gene regulation. Nat. Rev. Genet. 13, 505-516. doi: 10.1038/nrg3229
43. Roosens, N., Verbruggen, N., Meerts, P., Ximénez-Embún, P., and Smith, J. A. C. (2003). Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for sevel populations of Thlaspi caerulescensfrom Western Europe. Plant Cell Environ. 26, 1657-1672. doi: 10.1046/j.1365-3040.2003.01084.x
44. Schwartz, C., Echevarria, G., and Morel, J. L. (2003). Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249, 27-35. doi: 10.1023/A:1022584220411
45. Talke, I. N., Hanikenne, M., and Krämer, U. (2006). Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol. 142, 148-167. doi: 10.1104/pp.105.076232
46. Tolrà, R., Pongrac, P., Poschenrieder, C., Vogel-Mikuš, K., Regvar, M., and Barceló, J. (2006). Distinctive effects of cadmium on glucosinolate profiles in Cd hyperaccumulator Thlaspi praecox and non-hyperaccumulator Thlaspi arvense. Plant Soil 288, 333-341. doi: 10.1007/s11104-006-9124-1
47. Tusnády, G. E., and Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: applications to topology prediction. J. Mol. Biol. 283, 489-506. doi: 10.1006/jmbi.1998.2107
48. Tusnády, G. E., and Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850. doi: 10.1093/bioinformatics/17.9.849
49. van de Mortel, J. E., Schat, H., Moerland, P. D., Ver Looren van Themaat, E., van der Ent, S., Blankestijn, H., et al. (2008). Expression differences for genes involved in lignin, glutathione and sulfate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 31, 301-324. doi: 10.1111/j.1365-3040.2007.01764.x
50. van de Mortel, J. E., Villanueva, L. A., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P. D., et al. (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. 142, 1127-1147. doi: 10.1104/pp.106.082073
51. Vázquez, M. D., Barceló, J., Poschenrieder, C., Mádico, J., Hatton, P., Baker, A. J. M., et al. (1992). Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals. J. Plant Physiol. 140, 350-355. doi: 10.1016/S0176-1617(11)81091-6
52. Vogel-Mikuš, K., Drobne, D., and Regvar, M. (2005). Zn, Cd, and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ. Pollut. 133, 233-242. doi: 10.1016/j.envpol.2004.06.021
53. Wada, Y., Miyamoto, K., Kusano, T., and Sano, H. (2004). Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol. Genet. Genom. 271, 658-666. doi: 10.1007/s00438-004-1018-4
54. Weber, M., Harada, E., Vess, C., von Roepenack-Lahaye E., and Clemens, S. (2004). Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269-281. doi: 10.1046/j.1365-313X.2003.01960.x
55. White-Monsant, A. C., and Tang, C. (2013). Organic acids are not specifically involved in the nitrate-enhanced Zn hyperaccumulation mechanism in Noccaea caerulescens. Environ. Exp. Bot. 91, 12-21. doi: 10.1016/j.envexpbot.2013.02.006
56. Xing, J. P., Jiang, R. F., Ueno, D., Ma, J. F., Schat, H., McGrath, S. P., et al. (2008). Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens andThlaspi praecox. New Phytol. 178, 315-325. doi: 10.1111/j.1469-8137.2008.02376.x