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Cloning and characterization of phosphorus starvation inducible Brassica napus PURPLE ACID PHOSPHATASE 12 gene family, and imprinting of a recently evolved MITE-minisatellite twin structure

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Abstract

Purple acid phosphatase (PAP) is important for phosphorus assimilation and in planta redistribution. In this study, seven Brassica napus PAP12 (BnPAP12) genes orthologous to Arabidopsis thaliana PAP12 (AtPAP12) are isolated and characterized. NCBI BLASTs, multi-alignments, conserved domain prediction, and featured motif/residue characterization indicate that all BnPAP12 members encode dimeric high molecular weight plant PAPs. BnPAP12-1, BnPAP12-2, BnPAP12-3 and BnPAP12-7 (Group I) have six introns and encode 469-aa polypeptides structurally comparable to AtPAP12. BnPAP12-4 and BnPAP12-6 (Group II) have seven introns and encode 526-aa PAP12s. Encoding a 475-aa polypeptide, BnPAP12-5 (Group III) is evolved from a chimera of 5′ part of Group I and 3′ part of Group II. Sequence characterization and Southern detection suggest that there are about five BnPAP12 alleles. Homoeologous non-allelic fragment exchanges exist among BnPAP12 genes. BnPAP12-4 and BnPAP12-6 are imprinted with a Tourist-like miniature inverted-repeat transposable element (MITE) which is tightly associated with a novel minisatellite composed of four 36-bp tandem repeats. Existing solely in B. rapa/oleracea lineage, this recently evolved MITE-minisatellite twin structure does not impair transcription and coding capacity of the imprinted genes, and could be used to identify close relatives of B. rapa/oleracea lineage within Brassica. It is also useful for studying MITE activities especially possible involvement in minisatellite formation and gene structure evolution. BnPAP12-6 is silent in transcription. All other BnPAP12 genes basically imitate AtPAP12 in tissue specificity and Pi-starvation induced expression pattern, but divergence and complementation are distinct among them. Alternative polyadenylation and intron retention also exist in BnPAP12 mRNAs.

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Abbreviations

MITE:

Miniature inverted-repeat transposable element

MMTS:

MITE-minisatellite twin structure

PAP:

Purple acid phosphatase

References

  • Ast G (2004) How did alternative splicing evolve? Nat Rev Genet 5:773–782

    Article  PubMed  CAS  Google Scholar 

  • Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311:1–11

    Article  PubMed  CAS  Google Scholar 

  • Cavell AC, Lydiate DJ, Parkin IAP, Dean C, Trick M (1998) Collinearity between a 30-centimorgan segment of Arabidopsis thaliana chromosome 4 and duplicated regions within the Brassica napus genome. Genome 41:62–69

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Allona I, Rubio V, Leyva A, de la Pena A, Aragoncillo C, Paz-Ares J (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J 19:579–589

    Article  PubMed  CAS  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800

    Article  CAS  Google Scholar 

  • Durmus A, Eicken C, Sift BH, Kratel A, Kappl R, Huttermann J, Krebs B (1999a) The active site of purple acid phosphatase from sweet potatoes (Ipomoea batatas) metal content and spectroscopic characterization. Eur J Biochem 260:709–716

    Article  PubMed  CAS  Google Scholar 

  • Durmus A, Eicken C, Spener F, Krebs B (1999b) Cloning and comparative protein modeling of two purple acid phosphatase isozymes from sweet potatoes (Ipomoea batatas). Biochim Biophys Acta 1434:202–209

    PubMed  CAS  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable element: where genetics meets genomics. Nat Rev Genet 3:329–341

    Article  PubMed  CAS  Google Scholar 

  • Haran S, Logendra S, Seskar M, Bratanova M, Raskin I (2000) Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol 124:615–626

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DL (1950) The water culture method for growing plants without soil. Calif Agric Exp Sta Circ 347:32

    Google Scholar 

  • Jaakola L, Pirttil AM, Halonen M, Hohtola A (2001) Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Mol Biotechnol 19:201–203

    Article  PubMed  CAS  Google Scholar 

  • Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ (2005) Evolution of genome size in Brassicaceae. Ann Bot (Lond) 95:229–235

    Article  CAS  Google Scholar 

  • Klabunde T, Strater N, Krebs B, Witzel H (1995) Structural relationship between the mammalian Fe(III)–Fe(II) and the Fe(III)–Zn(II) plant purple acid phosphatases. FEBS Lett 367:56–60

    Article  PubMed  CAS  Google Scholar 

  • Kowalski SP, Lan TH, Feldmann KA, Paterson AH (1994) Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics 138:499–510

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Li DP, Zhu HF, Liu KF, Liu X, Leggewie G, Udvardi M, Wang DW (2002) Purple acid phosphatases of Arabidopsis thaliana: comparative analysis and differential regulation by phosphate deprivation. J Biol Chem 277:27772–27781

    Article  PubMed  CAS  Google Scholar 

  • Liao H, Wong FL, Phang TH, Cheung MY, Li WY, Shao G, Yan X, Lam HM (2003) GmPAP3, a novel purple acid phosphatase-like gene in soybean induced by NaCl stress but not phosphorus deficiency. Gene 318:103–111

    Article  PubMed  CAS  Google Scholar 

  • Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra Indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–1228

    PubMed  CAS  Google Scholar 

  • Olczak M, Morawiecka B, Watorek W (2003) Plant purple acid phosphatases—genes, structures and biological function. Acta Biochim Pol 50:1245–1256

    PubMed  CAS  Google Scholar 

  • Quiros CF, Grellet F, Sadowski J, Suzuki T, Li G, Wroblewski T (2001) Arabidopsis and Brassica comparative genomics sequence: structure and gene content in the ABI1-Rps2-Ck1 chromosomal segment and related regions. Genetics 157:1321–1330

    PubMed  CAS  Google Scholar 

  • Schenk G, Gahan LR, Carrington LE, Mitic N, Valizadeh M, Hamilton SE, de Jersey J, Guddat LW (2005) Phosphate forms an unusual tripodal complex with the Fe–Mn center of sweet potato purple acid phosphatase. Proc Natl Acad Sci USA 102:273–278

    Article  PubMed  CAS  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Article  PubMed  CAS  Google Scholar 

  • Skinner RJ, Todd AD (1998) Twenty-five years of monitoring pH and nutrient status of soils in England and Wales. Soil Use Man 14:162–169

    Google Scholar 

  • Singh K, Raizada J, Bhardwaj P, Ghawana S, Rani A, Singh H, Kaul K, Kumar S (2004) 26S rRNA-based internal control gene primer pair for reverse transcription-polymerase chain reaction-based quantitative expression studies in diverse plant species. Anal Biochem 335:330–333

    Article  PubMed  CAS  Google Scholar 

  • Strater N, Klabunde T, Tucker P, Witzel H, Krebs B (1995) Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)–Zn(II) active site. Science 268:1489–1492

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Wei YL, Li JN, Lu J, Tang ZL, Pu DC, Chai YR (2007) Molecular cloning of Brassica napus TRANSPARENT TESTA 2 gene family encoding potential MYB regulatory proteins of proanthocyanidin biosynthesis. Mol Biol Rep 34:105–120

    Article  PubMed  CAS  Google Scholar 

  • Xiao K, Harrison M, Wang ZY (2006) Cloning and characterization of a novel purple acid phosphatase gene (MtPAP1) from Medicago truncatula Barrel Medic. J Int Plant Biol 48:204–211

    Article  CAS  Google Scholar 

  • Zhu HF, Qian WQ, Lu XZ, Li DP, Liu X, Liu KF, Wang DW (2005) Expression patterns of purple acid phosphatase genes in Arabidopsis organs and functional analysis of AtPAP23 predominantly transcribed in flower. Plant Mol Biol 59:581–594

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Regierer B, Kossmann J, Frossard E, Amrhein N, Bucher M (2004) Differential expression of three purple acid phosphatases from potato. Plant Biol (Stuttg) 6:519–528

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are indebted to Professor Takeshi NISHIO, Laboratory Plant Breeding and Genetics, Graduate School of Agriculture, Tohoku University, Sendai, 981-8555, Japan, for kind provision of stock seeds of Brassicaceae species, and to Dr Genyi Li from University of Manitoba and Dr Guoping Chen from Chongqing University for critical reading of the manuscript. This research was supported by the National High Technology Research and Development Program of China (2006AA10A113 and 2006AA100106).

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Authors and Affiliations

  1. Chongqing Rapeseed Engineering Research Center, Southwest University, Tiansheng Road 216#, Beibei, Chongqing, 400716, P. R. China

    Kun Lu, You-Rong Chai, Kai Zhang, Rui Wang, Li Chen, Bo Lei, Jun Lu, Xin-Fu Xu & Jia-Na Li

  2. Chongqing Key Laboratory of Crop Quality Improvement, Southwest University, Tiansheng Road 216#, Beibei, Chongqing, 400716, P. R. China

    Kun Lu, You-Rong Chai, Kai Zhang, Rui Wang, Li Chen, Bo Lei, Jun Lu, Xin-Fu Xu & Jia-Na Li

  3. Key Laboratory of Biotechnology and Crop Quality Improvement of Ministry of Agriculture, Southwest University, Tiansheng Road 216#, Beibei, Chongqing, 400716, P. R. China

    Kun Lu, You-Rong Chai, Kai Zhang, Rui Wang, Li Chen, Bo Lei, Jun Lu, Xin-Fu Xu & Jia-Na Li

  4. College of Agronomy and Biotechnology, Southwest University, Tiansheng Road 216#, Beibei, Chongqing, 400716, P. R. China

    Kun Lu, You-Rong Chai, Kai Zhang, Rui Wang, Li Chen, Bo Lei, Jun Lu, Xin-Fu Xu & Jia-Na Li

Authors
  1. Kun Lu
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  2. You-Rong Chai
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  3. Kai Zhang
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  6. Bo Lei
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  7. Jun Lu
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  8. Xin-Fu Xu
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  9. Jia-Na Li
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Corresponding authors

Correspondence to You-Rong Chai or Jia-Na Li.

Additional information

Communicated by C. F. Quiros.

Kun Lu, You-Rong Chai and Jia-Na Li have equal contribution to the study.

Database Accession numbers: GenBank accession nos.: EU014612 (BnPAP12-1), EU014613 (BnPAP12-1 mRNA), EU014614 (BnPAP12-2), EU014615 (BnPAP12-2 mRNA), EU014616 (BnPAP12-3), EU014617 (BnPAP12-3 mRNA), EU014618 (BnPAP12-4), EU014619 (BnPAP12-4 mRNA), EU014620 (BnPAP12-4PM mRNA), EU014621 (BnPAP12-5), EU014622 (BnPAP12-5 mRNA), EU014623 (BnPAP12-5PM1 mRNA), EU014624 (BnPAP12-5PM2 mRNA), EU014625 (BnPAP12-6), EU014626 (BnPAP12-6 putative mRNA), EU014627 (BnPAP12-7), EU014628 (BnPAP12-7 mRNA) and EU014629 (BnPAP12-7PM mRNA).

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Lu, K., Chai, YR., Zhang, K. et al. Cloning and characterization of phosphorus starvation inducible Brassica napus PURPLE ACID PHOSPHATASE 12 gene family, and imprinting of a recently evolved MITE-minisatellite twin structure. Theor Appl Genet 117, 963–975 (2008). https://doi.org/10.1007/s00122-008-0836-x

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  • DOI: https://doi.org/10.1007/s00122-008-0836-x

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