Gene expression differences between noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation

Environmental Science and Technology

Volumn 48, Issue 6, 2014, Pages 3344-3353

  Halimaa, Pauliina ^a   Lin, Ya Fen ^c   Ahonen, Viivi H ^a   Blande, Daniel ^a   Clemens, Stephan ^d   Gyenesei, Attila ^b   Häikiö, Elina ^a   Kärenlampi, Sirpa O ^a   Laiho, Asta ^b   Aarts, Mark G M ^c   Pursiheimo, Juha Pekka ^b   Schat, Henk ^e   Schmidt, Holger ^d   Tuomainen, Marjo H ^a   Tervahauta, Arja I ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d UNIVERSITY OF BAYREUTH   (Germany)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOREMEDIATION; METAL IONS; NICKEL; PLANTS (BOTANY);

ANTI-OXIDANT ACTIVITIES; EXPRESSION PROFILE; GENE EXPRESSION DIFFERENCES; HIGH-THROUGHPUT SEQUENCING; HYPERACCUMULATION; INORGANIC CATIONS; NICKEL HYPERACCUMULATION; PHYTOREMEDIATION;

GENE EXPRESSION;

ANION; CADMIUM; CALCIUM ION; METAL; METAL ION; NICKEL; TRANSCRIPTOME; ZINC; HEAVY METAL; SOIL POLLUTANT; VEGETABLE PROTEIN;

ADAPTATION; ANTIOXIDANT; CATION; DICOTYLEDON; ECOTYPE; GENE EXPRESSION; HEAVY METAL; HYPERACCUMULATION; PHYTOREMEDIATION; POLLUTION TOLERANCE;

ANTIOXIDANT ACTIVITY; ARTICLE; ECOTYPE; GENE EXPRESSION; GENE ONTOLOGY; HIGH THROUGHPUT SEQUENCING; METAL TOLERANCE; NOCCAEA CAERULESCENS; NONHUMAN; PHENOTYPE; PHYTOREMEDIATION; PLANT GENE; PLANT ROOT; RNA SEQUENCE; THLASPI; BIOREMEDIATION; BRASSICACEAE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; SOIL POLLUTANT;

BIODEGRADATION, ENVIRONMENTAL; BRASSICACEAE; ECOTYPE; GENE EXPRESSION PROFILING; METALS, HEAVY; PLANT PROTEINS; SOIL POLLUTANTS; TRANSCRIPTOME;

EID: 84898947842     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es4042995     Document Type: Article

References (71)

1. Li, Y.; Chaney, R.; Brewer, E.; Roseberg, R.; Angle, J. S.; Baker, A.; Reeves, R.; Nelkin, J. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations Plant Soil 2003, 249 (1) 107-115
2. Chaney, R. L.; Angle, J. S.; Broadhurst, C. L.; Peters, C. A.; Tappero, R. V.; Sparks, D. L. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies J. Environ. Qual. 2007, 36 (5) 1429-1443
3. Hammond, J. P.; Bowen, H. C.; White, P. J.; Mills, V.; Pyke, K. A.; Baker, A. J. M.; Whiting, S. N.; May, S. T.; Broadley, M. R. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes New Phytol. 2006, 170 (2) 239-260
4. Weber, M.; Harada, E.; Vess, C.; Roepenack-lahaye, E. V.; Clemens, S. 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. 2004, 37 (2) 269-281
5. Becher, M.; Talke, I. N.; Krall, L.; Krämer, U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri Plant J. 2004, 37 (2) 251-268
6. van de Mortel, J. E.; Villanueva, L. A.; Schat, H.; Kwekkeboom, J.; Coughlan, S.; Moerland, P. D.; Ver Loren Van Themaat, E.; Koornneef, M.; Aarts, M. G. M. 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. 2006, 142 (3) 1127-1147
7. Plessl, M.; Rigola, D.; Hassinen, V. H.; Tervahauta, A.; Kärenlampi, S.; Schat, H.; Aarts, M. G. M.; Ernst, D. Comparison of two ecotypes of the metal hyperaccumulator Thlaspi caerulescens (J. & C. PRESL) at the transcriptional level Protoplasma 2010, 239 (1-4) 81-93
8. Rigola, D.; Fiers, M.; Vurro, E.; Aarts, M. G. M. The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis New Phytol. 2006, 170 (4) 753-766
9. Hassinen, V. H.; Tervahauta, A. I.; Halimaa, P.; Plessl, M.; Peräniemi, S.; Schat, H.; Aarts, M. G. M.; Servomaa, K.; Kärenlampi, S. O. Isolation of Zn-responsive genes from two accessions of the hyperaccumulator plant Thlaspi caerulescens Planta 2007, 225 (4) 977-989
10. Tuomainen, M. H.; Nunan, N.; Lehesranta, S. J.; Tervahauta, A. I.; Hassinen, V. H.; Schat, H.; Koistinen, K. M.; Auriola, S.; McNicol, J.; Kärenlampi, S. O. Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accessions Proteomics 2006, 6 (12) 3696-3706
11. Tuomainen, M.; Tervahauta, A.; Hassinen, V.; Schat, H.; Koistinen, K. M.; Lehesranta, S.; Rantalainen, K.; Häyrinen, J.; Auriola, S.; Anttonen, M.; Kärenlampi, S. Proteomics of Thlaspi caerulescens accessions and an inter-accession cross segregating for zinc accumulation J. Exp. Bot. 2010, 61 (4) 1075-1087
12. Milner, M. J.; Kochian, L. V. Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system Ann. Bot. 2008, 102 (1) 3-13
13. Roosens, N.; Verbruggen, N.; Meerts, P.; Ximénez-Embrún, P.; Smith, J. Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe Plant Cell Environ. 2003, 26 (10) 1657-1672
14. Zhao, F.; Hamon, R. E.; Lombi, E.; McLaughlin, M. J.; McGrath, S. P. Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens J. Exp. Bot. 2002, 53 (368) 535-543
15. Assunção, A. G.; Bookum, W. M.; Nelissen, H. J.; Vooijs, R.; Schat, H.; Ernst, W. H. Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types New Phytol. 2003, 159 (2) 411-419
16. Verbruggen, N.; Hermans, C.; Schat, H. Molecular mechanisms of metal hyperaccumulation in plants New Phytol. 2009, 181 (4) 759-776
17. Hassan, Z.; Aarts, M. G. M. Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants Environ. Exp. Bot. 2011, 72 (1) 53-63
18. Na, G.; Salt, D. E. The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants Environ. Exp. Bot. 2011, 72 (1) 18-25
19. Rascio, N.; Navari-Izzo, F. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci. 2011, 180 (2) 169-181
20. van de Mortel, J. E.; Aarts, M. G. M. Comparative transcriptomics-Model species lead the way New Phytol. 2006, 170 (2) 199-201
21. Roelofs, D.; Aarts, M. G. M.; Schat, H.; Van Straalen, N. M. Functional ecological genomics to demonstrate general and specific responses to abiotic stress Funct. Ecol. 2008, 22 (1) 8-18
22. Schat, H.; Vooijs, R.; Kuiper, E. Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris Evolution 1996, 50, 1888-1895
23. Anders, S.; Huber, W. Differential expression analysis for sequence count data Genome Biol. 2010, 11 (10) R106
24. R Development Core Team. R: A language and environment for statistical computing; R Foundation for Statistical Computing: Vienna, Austria, 2009.
25. Gentleman, R. C.; Carey, V. J.; Bates, D. M.; Bolstad, B.; Dettling, M.; Dudoit, S.; Ellis, B.; Gautier, L.; Ge, Y.; Gentry, J. Bioconductor: Open software development for computational biology and bioinformatics Genome Biol. 2004, 5 (10) R80
26. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat. Appl. Genet. Mol. Biol. 2004, 3 (1) 3
27. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing J. R. Stat. Soc. Ser. B 1995, 57, 289-300
28. David, M.; Dzamba, M.; Lister, D.; Ilie, L.; Brudno, M. SHRiMP2: Sensitive yet practical short read mapping Bioinformatics 2011, 27 (7) 1011-1012
29. Aboyoun, P.; Pages, H.; Lawrence, M. GenomicRanges: Representation and manipulation of genomic intervals. R package version 1.9.28; Bioconductor: 2012, http://www.bioconductor.org/.
30. Huang, D. W.; Sherman, B. T.; Lempicki, R. A. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 2009, 37 (1) 1-13
31. Huang, D. W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44-57
32. Min, X. J.; Butler, G.; Storms, R.; Tsang, A. OrfPredictor: Predicting protein-coding regions in EST-derived sequences Nucleic Acids Res. 2005, 33 (suppl 2) W677-W680
33. Conesa, A.; Götz, S.; García-Gómez, J. M.; Terol, J.; Talón, M.; Robles, M. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research Bioinformatics 2005, 21 (18) 3674-3676
34. Conesa, A.; Götz, S. Blast2GO: A comprehensive suite for functional analysis in plant genomics Int. J. Plant Genomics 2008, 10.1155/2008/619832
35. Götz, S.; García-Gómez, J. M.; Terol, J.; Williams, T. D.; Nagaraj, S. H.; Nueda, M. J.; Robles, M.; Talón, M.; Dopazo, J.; Conesa, A. High-throughput functional annotation and data mining with the Blast2GO suite Nucleic Acids Res. 2008, 36 (10) 3420-3435
36. Götz, S.; Arnold, R.; Sebastián-León, P.; Martín-Rodríguez, S.; Tischler, P.; Jehl, M.; Dopazo, J.; Rattei, T.; Conesa, A. B2G-FAR, a species-centered GO annotation repository Bioinformatics 2011, 27 (7) 919-924
37. Ueno, D.; Milner, M. J.; Yamaji, N.; Yokosho, K.; Koyama, E.; Clemencia Zambrano, M.; Kaskie, M.; Ebbs, S.; Kochian, L. V.; Ma, J. F. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens Plant J. 2011, 66 (5) 852-862
38. Craciun, A. R.; Meyer, C.; Chen, J.; Roosens, N.; De Groodt, R.; Hilson, P.; Verbruggen, N. Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation J. Exp. Bot. 2012, 63 (11) 4179-4189
39. Xing, J.; Jiang, R.; Ueno, D.; Ma, J.; Schat, H.; McGrath, S.; Zhao, F. Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox New Phytol. 2008, 178 (2) 315-325
40. R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2007.
41. Erban, A.; Schauer, N.; Fernie, A. R.; Kopka, J. Nonsupervised construction and application of mass spectral and retention time index libraries from time-of-flight gas chromatography-mass spectrometry metabolite profiles Metabolomics 2007, 358, 19-38
42. Schmidt, H.; Böttcher, C.; Trampczynska, A.; Clemens, S. Use of recombinantly produced 15N3-labelled nicotianamine for fast and sensitive stable isotope dilution ultra-performance liquid chromatography/electrospray ionization time-of-flight mass spectrometry Anal. Bioanal.Chem. 2011, 399 (3) 1355-1361
43. Gendre, D.; Czernic, P.; Conéjéro, G.; Pianelli, K.; Briat, J.; Lebrun, M.; Mari, S. TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter Plant J. 2007, 49 (1) 1-15
44. Richau, K. H.; Kozhevnikova, A. D.; Seregin, I. V.; Vooijs, R.; Koevoets, P. L.; Smith, J. A. C.; Ivanov, V. B.; Schat, H. Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens New Phytol. 2009, 183 (1) 106-116
45. Rogers, E. E.; Eide, D. J.; Guerinot, M. L. Altered selectivity in an Arabidopsis metal transporter Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (22) 12356-12360
46. Nishida, S.; Tsuzuki, C.; Kato, A.; Aisu, A.; Yoshida, J.; Mizuno, T. AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana Plant Cell Physiol. 2011, 52 (8) 1433-1442
47. Talke, I. N.; Hanikenne, M.; Krämer, U. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri Plant Physiol. 2006, 142 (1) 148-167
48. Schaaf, G.; Honsbein, A.; Meda, A. R.; Kirchner, S.; Wipf, D.; von Wirén, N. AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots J. Biol. Chem. 2006, 281 (35) 25532-25540
49. Montargès-Pelletier, E.; Chardot, V.; Echevarria, G.; Michot, L. J.; Bauer, A.; Morel, J. Identification of nickel chelators in three hyperaccumulating plants: An X-ray spectroscopic study Phytochemistry 2008, 69 (8) 1695-1709
50. Agrawal, B.; Lakshmanan, V.; Kaushik, S.; Bais, H. P. Natural variation among Arabidopsis accessions reveals malic acid as a key mediator of Nickel (Ni) tolerance Planta 2012, 236 (2) 477-489
51. Meyer, S.; Mumm, P.; Imes, D.; Endler, A.; Weder, B.; Al-Rasheid, K. A.; Geiger, D.; Marten, I.; Martinoia, E.; Hedrich, R. At ALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells Plant J. 2010, 63 (6) 1054-1062
52. Feng, W.; Benz, F. W.; Cai, J.; Pierce, W. M.; Kang, Y. J. Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress J. Biol. Chem. 2006, 281 (2) 681-687
53. Kerkeb, L.; Krämer, U. The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea Plant Physiol. 2003, 131 (2) 716-724
54. Dräger, D. B.; Desbrosses-Fonrouge, A.; Krach, C.; Chardonnens, A. N.; Meyer, R. C.; Saumitou-Laprade, P.; Krämer, U. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels Plant J. 2004, 39 (3) 425-439
55. Gustin, J. L.; Loureiro, M. E.; Kim, D.; Na, G.; Tikhonova, M.; Salt, D. E. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants Plant J. 2009, 57 (6) 1116-1127
56. Milner, M. J.; Craft, E.; Yamaji, N.; Koyama, E.; Ma, J. F.; Kochian, L. V. Characterization of the high affinity Zn transporter from Noccaea caerulescens, NcZNT1, and dissection of its promoter for its role in Zn uptake and hyperaccumulation New Phytol. 2012, 195 (1) 113-123
57. Courbot, M.; Willems, G.; Motte, P.; Arvidsson, S.; Roosens, N.; Saumitou-Laprade, P.; Verbruggen, N. A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase Plant Physiol. 2007, 144 (2) 1052-1065
58. Hanikenne, M.; Talke, I. N.; Haydon, M. J.; Lanz, C.; Nolte, A.; Motte, P.; Kroymann, J.; Weigel, D.; Krämer, U. Evolution of metal hyperaccumulation required cis -regulatory changes and triplication of HMA4 Nature 2008, 453 (7193) 391-395
59. Wojas, S.; Hennig, J.; Plaza, S.; Geisler, M.; Siemianowski, O.; Skłodowska, A.; Ruszczyńska, A.; Bulska, E.; Antosiewicz, D. M. Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation Environ. Pollut. 2009, 157 (10) 2781-2789
60. Deinlein, U.; Weber, M.; Schmidt, H.; Rensch, S.; Trampczynska, A.; Hansen, T. H.; Husted, S.; Schjoerring, J. K.; Talke, I. N.; Krämer, U.; Clemens, S. Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation Plant Cell 2012, 24 (2) 708-723
61. Clemens, S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants Biochimie 2006, 88 (11) 1707-1719
62. Birnbaum, K.; Shasha, D. E.; Wang, J. Y.; Jung, J. W.; Lambert, G. M.; Galbraith, D. W.; Benfey, P. N. A gene expression map of the Arabidopsis root Science 2003, 302 (5652) 1956-1960
63. Brady, S. M.; Orlando, D. A.; Lee, J.; Wang, J. Y.; Koch, J.; Dinneny, J. R.; Mace, D.; Ohler, U.; Benfey, P. N. A high-resolution root spatiotemporal map reveals dominant expression patterns Science 2007, 318 (5851) 801-806
64. Wu, J.; Zhao, F.-J.; Ghandilyan, A.; Logoteta, B.; Guzman, M. O.; Schat, H.; Wang, X.; Aarts, M. G. M. Identification and functional analysis of two ZIP metal transporters of the hyperaccumulator Thlaspi caerulescens Plant Soil 2009, 325 (1) 79-95
65. 2+-ATPase repertoire: Biochemical features and physiological functions Plant Biol. 2011, 13 (3) 421-430
66. Verbruggen, N.; Hermans, C.; Schat, H. Mechanisms to cope with arsenic or cadmium excess in plants Curr. Opin. Plant Biol. 2009, 12 (3) 364-372
67. Cailliatte, R.; Lapeyre, B.; Briat, J.; Mari, S.; Curie, C. The NRAMP6 metal transporter contributes to cadmium toxicity Biochem. J. 2009, 422, 217-228
68. Cailliatte, R.; Schikora, A.; Briat, J.; Mari, S.; Curie, C. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions Plant Cell 2010, 22 (3) 904-917
69. Takahashi, R.; Ishimaru, Y.; Senoura, T.; Shimo, H.; Ishikawa, S.; Arao, T.; Nakanishi, H.; Nishizawa, N. K. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice J. Exp. Bot. 2011, 62 (14) 4843-4850
70. Sasaki, A.; Yamaji, N.; Yokosho, K.; Ma, J. F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice Plant Cell 2012, 24 (5) 2155-2167
71. van de Mortel, J. E.; Schat, H.; Moerland, P. D.; Ver Loren Van Themaat, E.; Van Der Ent, S.; Blankestijn, H.; Ghandilyan, A.; Tsiatsiani, S.; Aarts, M. G. M. Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens Plant Cell Environ. 2008, 31 (3) 301-324