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Gene loss/retention and evolutionary pattern of ascorbic acid biosynthesis and recycling genes in Brassica rapa following whole genome triplication

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Abstract

Ascorbic acid (AsA) is an inevitable antioxidant found abundantly in higher plants. Despite the importance of AsA in plants, how AsA biosynthesis (ABGs; d-mannose/l-galactose pathway) and AsA recycling genes (ARGs) evolved through polyploidization has not been addressed to date. Here, we evaluated the impacts of whole genome triplication (WGT) on ABGs and ARGs in Chinese cabbage (Brassica rapa ssp. pekinensis), which diverged from Arabidopsis thaliana before the WGT event. Twenty-three ABGs coded in 13 loci representing nine different enzyme classes and 29 ARGs coded in 19 loci representing five different enzyme classes were identified in the B. rapa genome by whole-genome screening through comparative genomic analyses. Five of these loci maintained three gene copies, 10 loci maintained two gene copies and the majority of the loci (n = 17) maintained single gene copies. Segmental (62 %) and tandem duplication (6 %), and fragment (21 %) and large-scale recombination (10 %) events accelerated the diversification of ABGs and ARGs. Thirteen of the 52 (25 %) identified genes experienced intron losses and two (4 %) experienced intron gains implying that intron losses outnumbered intron gains. The expansion and the retention of ABGs and ARGs were similar to the whole genome gene expansion and retention (P > 0.05). These findings provide new insights into the structural characteristics and evolutionary trends of ABGs and ARGs. In addition, our data could become a useful resource to further the functional characterization of these genes.

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References

  • Babenko VN, Rogozin IB, Mekhedov SL, Koonin EV (2004) Prevalence of intron gain over intron loss in the evolution of paralogous gene families. Nucleic Acids Res 32:3724–3733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker MS, Kane NC, Matvienko M, Kozik A, Michelmore RW et al (2008) Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25:2445–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker MS, Baute GJ, Liu SL (2012) Duplications and turnover in plant genomes. In: Wandel et al (eds) Plant genome diversity, 1st edn. Springer, Vienna, pp 155–169

  • Bhatla N (2012) Exon-intron graphic maker. http://wormweb.org/exonintron. Accessed on 20 Dec 2015

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 8:422–433

    Google Scholar 

  • Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng F, Wu J, Fang L, Sun S, Liu B et al (2012) Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS ONE 7:e36442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng F, Manda´kova´ T, Wu J, Xie Q, Lysak MA et al (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25:1541–1554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin c) biosynthesis. Proc Natl Acad Sci USA 96:4198–4203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littlechild JA, Smirnoff N (2006) Arabidopsis thaliana VTC4 encodes l-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 281:15662–15670

    Article  CAS  PubMed  Google Scholar 

  • Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689

    Article  CAS  PubMed  Google Scholar 

  • Duan W, Song X, Liu T, Huan Z, Ren J, Hou X, Du J, Li Y (2015) Patterns of evolutionary conservation of ascorbic acid-related genes following whole-genome triplication in Brassica rapa. Genome Biol Evol 7:299–313

    Article  Google Scholar 

  • Finn RD, Bateman A, Clements A, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J et al (2014) The Pfam protein families database. Nucleic Acids Res 42:D222–D230

    Article  CAS  PubMed  Google Scholar 

  • Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443

    Article  CAS  PubMed  Google Scholar 

  • Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of l-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated l-galactose synthesis. Plant J 30:541–553

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Granlund I, Storm P, Schubert M, Garcia-Cerdan JG, Funk C et al (2009) The TL29 protein is lumen located, associated with PSII and not an ascorbate peroxidase. Plant Cell Physiol 50:1898–1910

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev 11:97–108

    Article  CAS  Google Scholar 

  • Jeffares DC, Mourier T, Penny D (2006) The biology of intron gain and loss. Trends Genet 22(1):16–22

    Article  CAS  PubMed  Google Scholar 

  • Kunz HH, Zamani-Nour S, Hausler RE, Ludewig K, Schroeder JI, Malinova I, Fettke J, Flugge UI, Gierth M (2014) Loss of cytosolic phosphoglucose isomerase affects carbohydrate metabolism in leaves and is essential for fertility of Arabidopsis. Plant Physiol 166:753–765

    Article  PubMed  PubMed Central  Google Scholar 

  • Leferink NGH, van den Berg WAM, van Berkel WJH (2008) l-galactono-γ-lactone dehydrogenase from Arabidopsis thaliana, a flavoprotein involved in vitamin C biosynthesis. FEBS J 275:713–726

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lim CK (2002) The function of ascorbate oxidase in Arabidopsis thaliana. PhD dissertation http://hdl.handle.net/10036/4077, University of Exeter. Accessed March 2015

  • Lisebnee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant memberane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914

    Article  Google Scholar 

  • Lundberg E, Storm P, Schroder WP, Funk C (2011) Crystal structure of the TL29 protein from Arabidopsis thaliana: an APX homolog without peroxidase activity. J Struct Biol 176:24–31

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Lemey P, Lott M, Moulton V, Posada D et al (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruta T, Yonemitsu M, Yabuta Y, Tamoi M, Ishikawa T et al (2008) Arabidopsis phosphomannose isomerase 1, but not phosphomannose isomerase 2, is essential for ascorbic acid biosynthesis. J Biol Chem 283:28842–28851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424

    Article  CAS  PubMed  Google Scholar 

  • Nishikimi M, Fukuyama R, Minoshima S, Shimizu N, Yagi K (1994) Cloning and chromosomal mapping of the human nonfunctional gene for L-gulonogamma-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J Biol Chem 269:13685–13688

    CAS  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Qian W, Yu C, Qin H, Liu X, Zhang A, Johansen IE, Wang D (2007) Molecular and functional analysis of phosphomannomutase (PMM) from higher plants and genetic evidence for the involvement of PMM in ascorbic acid biosynthesis in Arabidopsis and Nicotiana bentamiana. Plant J 49:399–413

    Article  CAS  PubMed  Google Scholar 

  • Qin C, Qian W, Wang W, Wu Y, Yu C, Jian X, Wang D, Wu P (2008) GDP-mannose pyrophosphorylase is a genetic determinant of ammonim sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:18308–18313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512

    Article  CAS  PubMed  Google Scholar 

  • Shi T, Huang H, Barker MS (2010) Ancient genome duplications during the evolution of kiwifruit (Actinidia) and related Ericales. Ann Bot 106:497–504

    Article  PubMed  PubMed Central  Google Scholar 

  • Smirnoff N (2011) Chapter 4 - Vitamin C: the metabolism and functions of ascorbic acid in plants. Adv Bot Res 59:107–177

    Article  CAS  Google Scholar 

  • Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH et al (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348

    Article  PubMed  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian C, Xiong Y, Liu T, Sun S, Chan L et al (2005) Evidence for an ancient whole-genome duplication event in rice and other cereals. Acta Genet Sin 32:519–527

    CAS  PubMed  Google Scholar 

  • Trivedi DK, Gill SS, Yadav S, Tuteja N (2013) Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis. Plant Signal Behav 8(2):e23201

    Article  Google Scholar 

  • Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K (2009) The flowering world: a tale of duplications. Trends Plant Sci 14:680–688

    Article  PubMed  Google Scholar 

  • Veitia RA (2005) Gene dosage balance: deletions, duplications and dominance. Trends Genet 21:33–35

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang H, Wang J, Sun R, Wu J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Wang YY, Hecker AG, Hauser BA (2014) The APX4 locus regulates seed vigor and seedling growth in Arabidopsis thaliana. Planta 239:909–919

    Article  CAS  PubMed  Google Scholar 

  • Wolucka BA, Montagu MV (2003) GDP-d-mannose-3′,5′-epimerase forms GDP-l-gulose, a putative intermediate for the de Novo biosynthesis of vitamin c in plants. J Biol Chem 278:47483–47490

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Tamaoki M, Shikano T, Nakajima N, Ogawa D, Ioki M, Aono M, Kubo A, Kamada H, Inoue Y, Saji H (2006) Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 47:304–308

    Article  CAS  PubMed  Google Scholar 

  • Yu TS, Lue WL, Wang SM, Chen J (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 123:319–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y (2013) Ascorbic acid in plants: biosynthesis, regulation and enhancement. Springer, New York

    Book  Google Scholar 

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Acknowledgments

This study was supported by the Postdoctoral Fellowship Program of the National Academy of Agricultural Science, the Rural Program for Agricultural Science and Technology Development (Project No.: PJ01002503), and by the Next-Generation Biogreen 21 Program (Project No.: PJ01116603), Rural Development Administration, Korea.

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  1. Panneerselvam Krishnamurthy

    Present address: Soybean Applied Genomics Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, 305-0856, Japan

Authors and Affiliations

  1. Department of Agricultural Biotechnology, National Institute of Agricultural Sciences (NAS), RDA, Jeonju, 54874, Korea

    Panneerselvam Krishnamurthy, Jin A. Kim, Mi-Jeong Jeong & Soo In Lee

  2. Department of Horticulture, Sunchon National University, Sunchon, 57922, Korea

    Ill Sup Nou

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  1. Panneerselvam Krishnamurthy
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Correspondence to Soo In Lee.

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Panneerselvam Krishnamurthy declares that he has no conflict of interest. Jin A Kim declares that she has no conflict of interest. Mi-Jeong Jeong declares that she has no conflict of interest. Ill Sup Nou declares that he has no conflict of interest. Soo In Lee declares that he has no conflict of interest.

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Krishnamurthy, P., Kim, J.A., Jeong, MJ. et al. Gene loss/retention and evolutionary pattern of ascorbic acid biosynthesis and recycling genes in Brassica rapa following whole genome triplication. Genes Genom 38, 1129–1143 (2016). https://doi.org/10.1007/s13258-016-0455-x

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