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Expansion and evolutionary patterns of GDSL-type esterases/lipases in Rosaceae genomes

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Abstract

GDSL-type esterase/lipase (GELP) is mainly characterized by a conserved GDSL domain at N terminus, and is widely found in all living species, both prokaryotes and eukaryotes. GELP gene family consists of a wide range of members playing important roles in plant physiological processes, such as development, stress responses, and functional divergences. In our study, 597 GELP genes were identified from six Rosaceae genomes (i.e., Fragaria vesca, Prunus persica, Prunus avium, Prunus mume, Pyrus bretschneideri, and Malus domestica) by a comprehensive analysis. All GELP genes were further divided into ten subfamilies based on phylogenetic tree analysis. Subfamily D and subfamily E are the two largest subfamilies. Microcollinearity analysis suggested that WGD/segmental events contribute to the expansion of the GELP gene family in M. domestica and P. bretschneideri compared to F. vesca, P. persica, P. avium, and P. mume. Some PbGELPs were expressed during the fruit development of P. bretschneideri and pollen tubes, indicating their activity in these tissues. The expression divergence of PbGELP duplication gene pairs suggests that many mutations were allowed during evolution, although the structure of GELP genes was highly conserved. The current study results provided the feasibility to understand the expansion and evolution patterns of GELP in Rosaceae genomes, and highlight the function during P. bretschneideri fruits and pollen tubes development.

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References

  • Akoh CC, Lee G-C, Liaw Y-C, Huang T-H, Shaw J-F (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43:534–552

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budak H, Zhang B (2017) MicroRNAs in model and complex organisms. Funct Integr Genomics 17:1–4

    Article  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(10):10

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao YP, Han Y, Jin Q, Lin Y, Cai Y (2016a) Comparative genomic analysis of the GRF genes in Chinese pear (Pyrus bretschneideri Rehd), poplar (populous), grape (Vitis vinifera), Arabidopsis and rice (Oryza sativa). Front Plant Sci 7:1750. https://doi.org/10.3389/fpls.2016.01750

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Han Y, Li D, Lin Y, Cai Y (2016b) MYB transcription factors in chinese pear (Pyrus bretschneideri Rehd.): genome-wide identification, classification, and expression profiling during fruit development. Front Plant Sci 7:577

  • Cao Y, Han Y, Meng D, Li D, Jiao C, Jin Q, Lin Y, Cai Y (2017) B-BOX genes: genome-wide identification, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri Rehd.). BMC Plant Biol 17:156. https://doi.org/10.1186/s12870-017-1105-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Han Y, Meng D, Abdullah M, Li D, Jin Q, Lin Y, Cai Y (2018) Systematic analysis and comparison of the PHD-finger gene family in Chinese pear (Pyrus bretschneideri) and its role in fruit development. Funct Integr Genomics. https://doi.org/10.1007/s10142-018-0609-9

    Article  CAS  Google Scholar 

  • Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85:63–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Xia R, Chen H, He Y (2018) TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface bioRxiv https://doi.org/10.1101/289660

  • Chepyshko H, Lai C-P, Huang L-M, Liu J-H, Shaw J-F (2012) Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: new insights from bioinformatics analysis. BMC Genomics 13:309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R, di Pierro EA, Gouzy J, Rees DJG, Guérif P, Muranty H, Durel CE, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, van de Weg E, Troggio M, Bucher E (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Yi H, Han C-T, Nou I-S, Hur Y (2016) GDSL esterase/lipase genes in Brassica rapa L.: genome-wide identification and expression analysis. Mol Gen Genomics 291:531–542

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faris JD, Zhang ZC, Fellers JP, Gill BS (2008) Micro-colinearity between rice, Brachypodium, and Triticum monococcum at the wheat domestication locus Q. Funct Integr Genomics 8:149–164

    Article  CAS  PubMed  Google Scholar 

  • Fawcett JA, Maere S, Van de Peer Y (2009) Plants with double genomes might have had a better chance to survive the cretaceous–tertiary extinction event. Proc Natl Acad Sci 106:5737–5742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fedorov A, Merican AF, Gilbert W (2002) Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc Natl Acad Sci 99:16128–16133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD et al (2013) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    Article  PubMed  PubMed Central  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD, Bairoch A (2005) Protein Identification and Analysis Tools on the ExPASy Server Proteomics Protocols Handbook 112:571–607

  • Ji R, Wang H, Xin X, Peng S, Hur Y, Li Z, Feng H (2017) BrEXL6, a GDSL lipase gene of Brassica rapa, functions in pollen development. Biol Plant 61:685–692

    Article  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282

    Article  CAS  Google Scholar 

  • Jung S et al (2013) The genome database for rosaceae (GDR): year 10 update. Nucleic Acids Res 42:D1237–D1244

    Article  PubMed  PubMed Central  Google Scholar 

  • Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, Suzuki K, Ishikawa A, Koshi T, Matsui R, Muto S, Matsui M (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147:1924–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kram BW, Bainbridge EA, Perera MAD, Carter C (2008) Identification, cloning and characterization of a GDSL lipase secreted into the nectar of Jacaranda mimosifolia. Plant Mol Biol 68:173–183

    Article  CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai C-P, Huang L-M, Chen L-FO, Chan M-T, Shaw J-F (2017) Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis. Plant Mol Biol 95:181–197

    Article  CAS  PubMed  Google Scholar 

  • Lee DS, Kim BK, Kwon SJ, Jin HC, Park OK (2009) Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling. Biochem Biophys Res Commun 379:1038–1042

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Jiang H, Zhou L, Deng L, Lin Y, Peng X, Yan H, Cheng B (2014) Molecular evolution of the HD-ZIP I gene family in legume genomes. Gene 533:218–228

    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 

  • Ling H et al (2006) Isolation and expression analysis of a GDSL-like lipase gene from Brassica napus L. J Biochem Mol Biol 39:297

    CAS  PubMed  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mistry J, Finn RD, Eddy SR, Bateman A, Punta M (2013) Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res 41:e121–e121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naranjo MA, Forment J, RoldÁN M, Serrano R, Vicente O (2006) Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell Environ 29:1890–1900

    Article  CAS  PubMed  Google Scholar 

  • Neilson J et al (2017) Gene expression profiles predictive of cold-induced sweetening in potato. Funct Integr Genomics 17:1–18

    Article  Google Scholar 

  • Oh IS, Park AR, Bae MS, Kwon SJ, Kim YS, Lee JE, Kang NY, Lee S, Cheong H, Park OK (2005) Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17:2832–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao X, Yin H, Li L, Wang R, Wu J, Wu J, Zhang S (2018) Different modes of gene duplication show divergent evolutionary patterns and contribute differently to the expansion of gene families involved in important fruit traits in pear (Pyrus bretschneideri). Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00161

  • Riemann M, Gutjahr C, Korte A, Riemann M, Danger B, Muramatsu T, Bayer U, Waller F, Furuya M, Nick P (2007) GER1, a GDSL motif-encoding gene from rice is a novel early light-and jasmonate-induced gene. Plant Biol 9:32–40

    Article  CAS  PubMed  Google Scholar 

  • Rodgers-Melnick E et al. (2011) Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res 22:95–105

    Article  PubMed  Google Scholar 

  • Shirasawa K, Isuzugawa K, Ikenaga M, Saito Y, Yamamoto T, Hirakawa H, Isobe S (2017) The genome sequence of sweet cherry (Prunus avium) for use in genomics-assisted breeding DNA Research:dsx020

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Salama DY (2010) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116. https://doi.org/10.1038/ng.740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488

    Article  CAS  PubMed  Google Scholar 

  • Updegraff EP, Zhao F, Preuss D (2009) The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sex Plant Reprod 22:197–204

    Article  CAS  PubMed  Google Scholar 

  • Upton C, Buckley JT (1995) A new family of lipolytic enzymes? Trends Biochem Sci 20:178–179

    Article  CAS  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus [times] domestica Borkh). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Verde I et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  PubMed  Google Scholar 

  • Volokita M, Rosilio-Brami T, Rivkin N, Zik M (2010) Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large GDSL-lipase family in land plants. Mol Biol Evol 28:551–565

    Article  PubMed  Google Scholar 

  • Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49–e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang X, Tang H, Tan X, Ficklin SP, Feltus FA, Paterson AH (2011) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 6:e28150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Ding Z, Vizcay-Barrena G, Shi J, Liang W, Yuan Z, Werck-Reichhart D, Schreiber L, Wilson ZA, Zhang D (2014) ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26:1544–1556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yim WC, Lee B-M, Jang CS (2009) Expression diversity and evolutionary dynamics of rice duplicate genes. Mol Gen Genomics 281:483–493

    Article  CAS  Google Scholar 

  • Zdobnov EM, Apweiler R (2001) InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Chen W, Sun L, Zhao F, Huang B, Yang W, Tao Y, Wang J, Yuan Z, Fan G, Xing Z, Han C, Pan H, Zhong X, Shi W, Liang X, du D, Sun F, Xu Z, Hao R, Lv T, Lv Y, Zheng Z, Sun M, Luo L, Cai M, Gao Y, Wang J, Yin Y, Xu X, Cheng T, Wang J (2012) The genome ofPrunus mume. Nat Commun 3:1318

    Article  PubMed  Google Scholar 

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Acknowledgments

We extend our thanks to the reviewers and editors for their careful reading and helpful comments on this manuscript.

Funding

This study was supported by The National Natural Science Foundation of China (grant 31640068).

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Contributions

YCao designed and performed the experiments. YCao, DM, and YH analyzed the data. YH, DM, YL, QJ, DL, JY, YCao, AM, and YCai contributed reagents/materials/analysis tools. YCao and YH wrote the paper. All authors reviewed and approved this submission.

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Correspondence to Yongping Cai.

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The authors declare that they have no competing interests.

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Figure S1

The Maximum Likelihood tree for GELP genes identified among the six Rosaceae genomes. Totally, 597 GELP genes were divided into ten subfamilies (A-J), and were indicated by different colors. (PNG 699 kb)

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(TIF 3080 kb)

Figure S2

The phylogenetic tree for GELP genes identified in six Rosaceae genomes. Subfamilies are numbered at the right part of the ML tree and marked with alternating tones to facilitate subfamily identification. (PNG 4633 kb)

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(TIF 6556 kb)

Figure S3

Motif logo of four conserved blocks found in Rosaceae GELP proteins: I (a), II (b), III (c), and V (d). The red triangles indicate conserved residues Ser-Gly-Asn-His in blocks. In the present study, the full-length GELP protein sequences were submitted to MEME website to scan conserved motifs in these proteins, based on previous research manuscripts (Dong et al. 2016). (PNG 1060 kb)

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(TIF 660 kb)

Figure S4

Exon–intron structure analysis of Rosaceae GELP genes. The scale represents the length of the DNA sequence. Legend is at the top right of the Figure. (PNG 3048 kb)

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(TIF 4507 kb)

Figure S5

Heat map of P. bretschneideri GELP genes in different tissues, including MP (Mature pollen grains), HP (Hydrated pollen grains), PT (Pollen tube), SPT (Stop-growth pollen tube), fruit_stage1 (15 days after full blooming (DAB)), fruit_stage2 (30 DAB), fruit_stage3 (55 DAB), fruit_stage4 (85 DAB), fruit_stage5 (115 DAB), fruit_stage6 (mature stage), and fruit_stage7 (fruit senescence stage), and PbGELP gene expression levels in different conditions, including pear leaf with inoculated distilled water (Leaf_CK), pear leaf with inoculated black spot (Alternarlia alternate) 2 (Leaf_T2), pear leaf with inoculated black spot (Alternarlia alternate) 3 (Leaf_T3), pear fruit with no any treatment (Fruit_CK), pear fruit with Gibberellins treatment (Fruit_GA), pear with salt treatment (Leaf_Salt), pear fruit pericarp-russet (pericarp-russet), and pear fruit pericarp-green (pericarp-green). Blue and red colors correspond to down-regulation and up-regulation, respectively. (PNG 210 kb)

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(TIF 358 kb)

Figure S6

The Maximum likelihood tree of GELP genes in six Rosaceae species, Arabidopsis and rice. (PDF 87 kb)

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Cao, Y., Han, Y., Meng, D. et al. Expansion and evolutionary patterns of GDSL-type esterases/lipases in Rosaceae genomes. Funct Integr Genomics 18, 673–684 (2018). https://doi.org/10.1007/s10142-018-0620-1

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