Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large gdSL-lipase family in land plants

Molecular Biology and Evolution

Volumn 28, Issue 1, 2011, Pages 551-565

  Volokita, Micha ^a   Rosilio Brami, Tamar ^a   Rivkin, Natalia ^a   Zik, Moriyah ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

GDSL lipase; gene family phylogeny; intron gain and loss; land plants; syntany

Indexed keywords

DNA; TRIACYLGLYCEROL LIPASE;

ARTICLE; BIOTRANSFORMATION; DNA TRANSPOSITION; GENE DUPLICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ANALYSIS; INTRON; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLANT GENE; SYNTENY;

AMINO ACID SEQUENCE; BASE SEQUENCE; CARBOXYLIC ESTER HYDROLASES; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENETIC SPECIATION; GENOME; INTRONS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PLANT PROTEINS; PLANTS; SEQUENCE ALIGNMENT; SYNTENY;

BRYOPHYTES; EMBRYOPHYTA; GYMNOSPERMAE; LILIOPSIDA;

EID: 78650428395     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq226     Document Type: Article

References (68)

1. Abdelkafi S, Ogata H, Barouh N, Fouquet B, Lebrun R, Pina M, Scheirlinckx F, Villeneuve P, Carriere F. 2009. Identification and biochemical characterization of a GDSL-motif carboxylester hydrolase from Carica papaya latex. Biochim Biophys Acta. 1791:1048-1056.
2. Agee AE, Surpin M, Sohn EJ, et al. (14 co-authors). 2010. MODIFIED VACUOLE PHENOTYPE1 is an Arabidopsis myrosinase-associated protein involved in endomembrane protein trafficking. Plant Physiol. 152:120-132.
3. Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF. 2004. GDSL family of serine esterases/lipases. Prog Lipid Res. 43:534-552.
4. Angkawidjaja C, Kanaya S. 2006. Family I.3 lipase: bacterial lipases secreted by the type I secretion system. Cell Mol Life Sci. 63:2804-2817.
5. Arif SA, Hamilton RG, Yusof F, Chew NP, Loke YH, Nimkar S, Beintema JJ, Yeang Hy. 2004. Isolation and characterization of the earlynnodule-specific protein homologue (Hev b 13), an allergenic lipolyic esterase from Hevea brasiliensis latex. J Biol Chem. 279:23933-23941.
6. 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.
7. Blanc G, Wolfe KH. 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell. 16:1679-1691.
8. Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL. 2004. WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA. 101: 4706-4711.
9. Brunner AM, Busov VB, Strauss SH. 2004. Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci. 9:49-56.
10. 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.
11. Cao D, Cheng H, Wu W, Soo HM, Peng J. 2006. Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol. 142:509-525.
12. Clauss K, Baumert A, Nimtz M, Milkowski C, Strack D. 2008. Role of a GDSL lipase-like protein as sinapine esterase in Brassicaceae. Plant J. 53:802-813.
13. Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C. 2008. Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J. 53:53-64.
14. Dickstein R, Prusty R, Peng T, Ngo W, Smith ME. 1993. ENOD8, a novel early nodule-specific gene, is expressed in empty alfalfa nodules. Mol Plant Microbe Interact. 6:715-721.
15. Fedorov A, Merican AF, Gilbert W. 2002. Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc Natl Acad Sci USA. 99:16128-16133.
16. Feiber AL, Rangarajan J, Vaughn JC. 2002. The evolution of single-copy Drosophila nuclear 4f-rnp genes: spliceosomal intron losses create polymorphic alleles. J Mol Evol. 55:401-413.
17. Gonnet GH, Cohen MA, Benner SA. 1992. Exhaustive matching of the entire protein sequence database. Science 256:1443-1445.
18. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
19. Hong JK, Choi HW, Hwang IS, Kim DS, Kim NH, Choi du S, Kim YJ, Hwang BK. 2008. Function of a novel GDSL-type pepper lipase gene, CaGLIP1, in disease susceptibility and abiotic stress tolerance. Planta 227:539-558.
20. Initiative TAG. 2000. Analysis of the genome sequence of the flowering plant. Arabidopsis thaliana. Nature 408:796-815.
21. Jaillon O, Aury J-M, Noel B, et al. (56 co-authors). 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467.
22. Kandzia R, Grimm R, Eckerskorn C, Lindemann P, Luckner M. 1998. Purification and characterization of lanatoside 15'-O-acetylesterase from Digitalis lanata Ehrh. Planta 204:383-389.
23. Kannangara R, Branigan C, Liu Y, et al. 2007. The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell. 19:1278-1294.
24. Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T. 2005. Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His-.Asp phosphorelay circuitry. Plant Cell Physiol. 46:339-355.
25. Kim KJ, Lim JH, Kim MJ, Kim T Chung HM, Paek KH. 2008. GDL-lipase 1 (CaGL1) contributes to wound stress resistance by modulation of CaPR-4 expression in hot pepper. Biochem Biophys Res Commun. 374:693-698.
26. Kondou Y, Nakazawa M, Kawashima M, et al. 2008. RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol. 147:1924-1935.
27. Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, De Pamphilis CW. 2007. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J. 50:873-885.
28. Koonin EV. 2005. Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet. 39:309-338.
29. Kram BW, Bainbridge EA, Perera MA, Carter C. 2008. Identification, cloning and characterization of a GDSL lipase secreted into the nectar of Jacaranda mimosifolia. Plant Mol Biol. 68: 173-183.
30. Kwon SJ, Jin HC, Lee S, Nam MH, Chung JH, Kwon SI, Ryu C-M, Park OK. 2009. GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J. 58:235-245.
31. Lee K-A, Cho T-J. 2003. Characterization of a salicylic acid- and pathogen-induced lipase-like gene in chinese cabbage. J Biochem Mol Biol. 36:433-441.
32. Lyons E, Freeling M. 2008. How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53:661-673.
33. Lyons E, Pedersen B, Kane J, et al. 2008. Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol. 148: 1772-1781.
34. Mayer K, Murphy G, Tarchini R, et al. (18 co-authors). 2001. Conservation of microstructure between a sequenced region of the genome of rice and multiple segments of the genome of Arabidopsis thaliana. Genome Res. 11:1167-1174.
35. Mayfield JA, Fiebig A, Johnstone SE, Preuss D. 2001. Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292:2482-2485.
36. Mintz-Oron S, Mandel T, Rogachev I, et al. (11 co-authors). 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol 147:823-851.
37. Moore RC, Purugganan MD. 2005. The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol. 8:122-128.
38. Naranjo MA, Forment J, Roldan 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.
39. Ner-Gaon H, Leviatan N, Rubin E, Fluhr R. 2007. Comparative cross-species alternative splicing in plants. Plant Physiol. 144:1632-1641.
40. O'Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I. 2008. On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol. 25:1120-1128.
41. Oh IS, Park AR, Bae MS, et al. (10 co-authors). 2005. Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell. 17:2832-2847.
42. Omilian AR, Scofield DG, Lynch M. 2008. Intron presence-absence polymorphisms in Daphnia. Mol Biol Evol. 25:2129-2139.
43. Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A. 2010. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant. 3:563-575.
44. Paterson AH, Bowers JE, Bruggmann R, et al. (45 co-authors). 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457:551-556.
45. Project IRGS. 2005. The map-based sequence of the rice genome. Nature 436:793-800.
46. Ralph SG, Chun HJ, Kolosova N, et al. (15 co-authors). 2008. A conifer genomics resource of 200,000 spruce (Picea spp.) ESTs and 6,464 high-quality, sequence-finished full-length cDNAs for Sitka spruce (Picea sitchensis). BMC Genomics. 9:484.
47. Reina JJ, Guerrero C, Heredia A. 2007. Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. J Exp Bot. 58:2717-2731.
48. Rensing SA, Lang D, Zimmer AD, et al. (70 co-authors). 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64-69.
49. Riemann M, Gutjahr C, Korte A, et al. (10 co-authors). 2007. GER1, a GDSL motif-encoding gene from rice is a novel early light- and jasmonate-induced gene. Plant Biol. 9:32-40.
50. Roy SW, Fedorov A, Gilbert W. 2003. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci USA. 100:7158-7162.
51. Sagane Y, Nakagawa T, Yamamoto K, Michikawa S, Oguri S, Momonoki YS. 2005. Molecular characterization of maize acetyl-cholinesterase: a novel enzyme family in the plant kingdom. Plant Physiol. 138:1359-1371.
52. Sampedro J, Lee Y, Carey RE, dePamphilis C, Cosgrove DJ. 2005. Use of genomic history to improve phylogeny and understanding of births and deaths in a gene family. Plant J. 44:409-419.
53. Sappl PG, Heazlewood JL, Millar AH. 2004. Untangling multi-gene families in plants by integrating proteomics into functional genomics. Phytochemistry 65:1517-1530.
54. Sharpton T, Neafsey D, Galagan J, Taylor J. 2008. Mechanisms of intron gain and loss in Cryptococcus. Genome Biol. 9:R24.
55. Soltis DE, Albert VA, Leebens-Mack J, et al. (10 co-authors). 2009. Polyploidy and angiosperm diversification. Am J Bot. 96: 336-348.
56. Soltis PS, Soltis DE, Chase MW. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402-404.
57. Stoltzfus A, Logsdon JM Jr, Palmer JD, Doolittle WF. 1997. Intron "sliding" and the diversity of intron positions. Proc Natl Acad Sci USA. 94:10739-10744.
58. Taipalensuu J, Andreasson E, Eriksson S, Rask L. 1997. Regulation of the wound-induced myrosinase-associated protein transcript in Brassica napus plants. Eur J Biochem. 247:963-971.
59. Taipalensuu J, Falk A, Rask L. 1996. A wound- and methyl jasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin. Plant Physiol. 110:483-491.
60. Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, Nishimura M, Hara-Nishimura I. 2010. Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. Plant Cell Physiol. 51:123-131.
61. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599.
62. Tuskan GA, Difazio S, Jansson S, et al. (110 co-authors). 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596-1604.
63. 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.
64. Upton C, Buckley JT. 1995. A new family of lipolytic enzymes? Trends Biochem Sci. 20:178-179.
65. Venkatesh B, Ning Y, Brenner S. 1999. Late changes in spliceosomal introns define clades in vertebrate evolution. Proc Natl Acad Sci USA. 96:10267-10271.
66. Wang W, Zheng H, Fan C, et al. (14 co-authors). 2006. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell. 18:1791-1802.
67. Yamamoto K, Oguri S, Momonoki YS. 2008. Characterization of trimeric acetylcholinesterase from a legume plant, Macroptilium atropurpureum Urb. Planta. 227: 809-822.
68. Zhang Z, Ober JA, Kliebenstein DJ. 2006. The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell. 18:1524-1536.