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Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator noccaea caerulescens

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Ó Lochlainn, Seosamh, Bowen, Helen C., Fray, R. G. , Hammond, John P., King, Graham J., White, Philip J., Graham, Neil S. and Broadley, Martin R.. (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator noccaea caerulescens. PL o S One, Vol.6 (No.3). e17814. ISSN 1932-6203

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Official URL: http://dx.doi.org/10.1371/journal.pone.0017814

Abstract

Zinc (Zn) and cadmium (Cd) hyperaccumulation may have evolved twice in the Brassicaceae, in Arabidopsis halleri and in the Noccaea genus. Tandem gene duplication and deregulated expression of the Zn transporter, HMA4, has previously been linked to Zn/Cd hyperaccumulation in A. halleri. Here, we tested the hypothesis that tandem duplication and deregulation of HMA4 expression also occurs in Noccaea. A Noccaea caerulescens genomic library was generated, containing 36,864 fosmid pCC1FOSTM clones with insert sizes ~20–40 kbp, and screened with a PCR-generated HMA4 genomic probe. Gene copy number within the genome was estimated through DNA fingerprinting and pooled fosmid pyrosequencing. Gene copy numbers within individual clones was determined by PCR analyses with novel locus specific primers. Entire fosmids were then sequenced individually and reads equivalent to 20-fold coverage were assembled to generate complete whole contigs. Four tandem HMA4 repeats were identified in a contiguous sequence of 101,480 bp based on sequence overlap identities. These were flanked by regions syntenous with up and downstream regions of AtHMA4 in Arabidopsis thaliana. Promoter-reporter b-glucuronidase (GUS) fusion analysis of a NcHMA4 in A. thaliana revealed deregulated expression in roots and shoots, analogous to AhHMA4 promoters, but distinct from AtHMA4 expression which localised to the root vascular tissue. This remarkable consistency in tandem duplication and deregulated expression of metal transport genes between N. caerulescens and A. halleri, which last shared a common ancestor >40 mya, provides intriguing evidence that parallel evolutionary pathways may underlie Zn/Cd hyperaccumulation in Brassicaceae.

Item Type: Journal Article
Subjects: Q Science > QK Botany
Divisions: Faculty of Science > Life Sciences (2010- )
Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH): Hyperaccumulator plants -- Genetics, Cruciferae -- Genetics, Zinc, Cadmium
Journal or Publication Title: PL o S One
Publisher: Public Library of Science
ISSN: 1932-6203
Date: 10 March 2011
Volume: Vol.6
Number: No.3
Page Range: e17814
Identification Number: 10.1371/journal.pone.0017814
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
Funder: Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Scotland. Rural and Environment Research and Analysis Directorate (RERAD)
Grant number: BBSSE200613215 (BBSRC)
References: 1. White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Annals of Botany 105: 1073–1080. 2. Mills RF, Francini A, Ferreira da Rocha PSC, Baccarini PJ, Aylett M, et al. (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Letters 579: 783–791. 3. Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Current Opinion in Plant Biology 9: 322–330. 4. Kra¨mer U, Talke, IN, Hanikenne M (2007) Transition metal transport. FEBS Letters 581: 2263–2272. 5. Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytologist 174: 499–506. 6. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist 182: 49–84. 7. Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant Journal 35: 164–176. 8. Verret F, Gravot A, Auroy P, Leonhardt N, David P, et al. (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Letters 576: 306–312. 9. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, et al. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. The Plant Cell 16: 1327–1339. 10. Verret F, Gravot A, Auroy P, Preveral S, Forestier C, et al. (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Letters 579: 1515–1522. 11. Wong CK, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot translocation in Arabidopsis thaliana. New Phytologist 181: 71–78. 12. Sinclair SA, Sherson SM, Jarvis R, Camakaris J, Cobbett CS (2007) The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytologist 174: 39–45. 13. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytologist 173: 677–702. 14. Kra¨mer U (2010) Metal hyperaccumulation in plants. Annual Review of Plant Biology 61: 517–534. 15. Macnair MR (2003) The hyperaccumulation of metals by plants. Advances in Botanical Research 40: 63–105. 16. Taylor SI (2004) Evolution of Zinc Hyperaccumulation in Thlaspi. Exeter, UK: PhD. University of Exeter. 17. Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, et al. (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytologist 159: 421–430. 18. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, et al. (2007) A major quantitative trait locus for Cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology 144: 1052–1065. 19. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453: 391–395. 20. Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiology 136: 3814–3823. 21. Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, et al. (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytologist 170: 239–260. 22. Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Letters 569: 140–148. 23. van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, et al. (2006) Large expression differences in genes for iron and zinc homeostatis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 142: 1127–1147. 24. Kim UJ, Shizuya H, de Jong PJ, Birren B, Simon MI (1992) Stable propagation of cosmid sized human DNA inserts in an F factor based vector. Nucleic Acids Research 20: 1083–1085. 25. Wang X, Zhang Q, Sun X, Chen Y, Zhai T, et al. (2009) Fosmid library construction and initial analysis of end sequences in female half-smooth tongue sole (Cynoglossus semilaevis). Marine Biotechnology 11: 236–242. 26. Wild J, Hradecna Z, Szybalski W (2002) Conditionally amplifiable BACs: Switching from single-copy to high-copy vectors and genomic clones. Genomic Research 12: 1434–1444. 27. Nyre´n P (2007) The History of Pyrosequencing. Methods in Molecular Biology 373: 1–13. 28. Meyer M, Stenzel U, Hofreiter M (2008) Parallel tagged sequencing on the 454 platform. Nature Protocols 3: 267–278. 29. Pettersson E, Lundeberg J, Ahmadian A (2009) Generations of sequencing technologies. Genomics 93: 105–111. 30. O ´ Lochlainn S, Fray RG, Hammond JP, King GJ, White PJ, et al. (2011) Generation of nonvernal-obligate, faster-cycling Noccaea caerulescens lines through fast neutron mutagenesis. New Phytologist 189: 409–414. 31. Riley R (1956) The influence of the breeding system on the genecology of Thlaspi alpestre L. New Phytologist 55: 319–330. 32. Pollard AJ, Baker AJM (1996) Quantitative genetics of zinc hyperaccumulation in Thlaspi caerulescens. New Phytologist 132: 113–118. 33. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist 145: 11–20. 34. Jime´nez-Ambriz G, Petit C, Bourrie´ I, Dubois S, Olivieri I, et al. (2007) Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: role of gene flow, selection and phenotypic plasticity. New Phytologist 173: 199–215. 35. Munamenhof K, Koch M (1994) Chloroplast DNA restriction site variation and phylogenetic relationships in the genus Thlaspi sensu lato (Brassicaceae). Systematic Botany 19: 73–88. 36. Koch M, Mummenhoff K, Hurka H (1998) Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: Evidence from genetic studies based on isozyme analysis. Biochemical Systematic and Ecology 26: 823–838. 37. Dubois S, Cheptou PO, Petit C, Meerts P, Poncelet M, et al. (2003) Genetic structure and mating system of metallicolous and nonmetallicolous populations of Thlaspi caerulescens. New Phytologist 157: 633–641. 38. Higgins K, Lynch M (2001) Metapopulation extinction caused by mutation accumulation. Proceedings of the National Academy of Sciences of the United States of America 98: 2928–2933. 39. Roze D, Rousset F (2004) Joint effects of self-fertilization and population structure on mutation load, inbreeding depression and heterosis. Genetics 167: 1001–1015. 40. Bikard D, Patel D, Le Mette C, Giorgi V, Camilleri C, et al. (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323: 623–626. 41. Santuari L, Pradervand S, Amiguet-Vercher AM, Thomas J, Dorcey E, et al. (2010) Substantial deletion overlap among divergent Arabidopsis genomes revealed by intersection of short reads and tiling arrays. Genome Biology 11: R4. 42. Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, et al. (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Research 20: 1689–1699. 43. Mills RF, Valdes B, Duke M, Peaston KA, Lahner B, et al. (2010) Functional significance of AtHMA4 C-Terminal domain in planta. PLoS ONE 5: e13388. doi:10.1371/journal.pone.0013388. 44. Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. PNAS 107: 18724–18728. 45. Talke IN, Hanikenne M, Kra¨mer 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 Physiology 142: 148–167. 46. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220: 731–736. 47. Frey B, Keller C, Zierold K, Schulin R (2000) Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant, Cell and Environment 23: 675–687. 48. Ku¨pper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212: 75–84. 49. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual (third edition). Cold Spring HarborNew York: Cold Spring Harbor Laboratory Press. 50. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of Bioscience and Bioengineering 104: 34–41. 51. Koncz C, Schell J (1986) The promoter of the TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Molecular and General Genetics 204: 383–396. 52. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: b-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6: 3901–3907. 53. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant Journal 16: 735–743.
URI: http://wrap.warwick.ac.uk/id/eprint/34581

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