期刊论文详细信息
BMC Genomics
Genome-wide and molecular evolution analysis of the subtilase gene family in Vitis vinifera
Xiangyang Hu1  Jinling Huang2  Yongping Yang1  Ticao Zhang1  Xi Han3  Jun Cao4 
[1] The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China;Department of Biology, East Carolina University, Greenville, NC 27858, USA;University of Chinese Academy of Sciences, Beijing, China;Institute of Life Sciences, Jiangsu University, Zhenjiang, Jiangsu 212013, China
关键词: Differential expression;    Positive selection;    Evolution;    Gene family;    Subtilase;    Vitis vinifera;   
Others  :  1127226
DOI  :  10.1186/1471-2164-15-1116
 received in 2014-04-11, accepted in 2014-12-11,  发布年份 2014
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【 摘 要 】

Background

Vitis vinifera (grape) is one of the most economically significant fruit crops in the world. The availability of the recently released grape genome sequence offers an opportunity to identify and analyze some important gene families in this species. Subtilases are a group of subtilisin-like serine proteases that are involved in many biological processes in plants. However, no comprehensive study incorporating phylogeny, chromosomal location and gene duplication, gene organization, functional divergence, selective pressure and expression profiling has been reported so far for the grape.

Results

In the present study, a comprehensive analysis of the subtilase gene family in V. vinifera was performed. Eighty subtilase genes were identified. Phylogenetic analyses indicated that these subtilase genes comprised eight groups. The gene organization is considerably conserved among the groups. Distribution of the subtilase genes is non-random across the chromosomes. A high proportion of these genes are preferentially clustered, indicating that tandem duplications may have contributed significantly to the expansion of the subtilase gene family. Analyses of divergence and adaptive evolution show that while purifying selection may have been the main force driving the evolution of grape subtilases, some of the critical sites responsible for the divergence may have been under positive selection. Further analyses of real-time PCR data suggested that many subtilase genes might be important in the stress response and functional development of plants.

Conclusions

Tandem duplications as well as purifying and positive selections have contributed to the functional divergence of subtilase genes in V. vinifera. The data may contribute to a better understanding of the grape subtilase gene family.

【 授权许可】

   
2014 Cao et al.; licensee BioMed Central.

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【 参考文献 】
  • [1]Siezen RJ, Leunissen JA: Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci 1997, 6:501-523.
  • [2]Antao CM, Malcata FX: Plant serine proteases: biochemical, physiological and molecular features. Plant Physiol Biochem 2005, 43:637-650.
  • [3]Dodson G, Wlodawer A: Catalytic triads and their relatives. Trends Biochem Sci 1998, 23:347-352.
  • [4]Siezen RJ, Renckens B, Boekhorst J: Evolution of prokaryotic subtilases: genome-wide analysis reveals novel subfamilies with different catalytic residues. Proteins 2007, 67(3):681-994.
  • [5]Fuller RS, Brake A, Thorner J: Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2_-dependent serine protease. Proc Natl Acad Sci U S A 1989, 86:1434-1438.
  • [6]Seidah NGKA, Prat A: The proprotein convertases and their implication in sterol and/or lipid metabolism. Biol Chem 2006, 387:871-877.
  • [7]Schaller A, Stintzi A, Graff L: The family of subtilisin/kexin like pro-protein and pro-hormone convertases: Divergent or shared functions. Biochimie 1994, 76:197-209.
  • [8]Seidah NG, Chrétien M: Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 1999, 848(1–2):45-62.
  • [9]Yamagata H, Masuzawa T, Nagaoka Y, Ohnishi T, Iwasaki T: cucumisin, a serine protease from melon fruits, shares structural homology with subtilisin and is generated from a large precursor. J Biol Chem 1994, 269:32725-32731.
  • [10]Ribeiro A, Akkermans ADL, van Kammen A, Bisseling T, Pawlowski K: A nodule-specific gene encoding a subtilisin like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 1995, 7:785-794.
  • [11]Taylor AA, Horsch A, Rzepczyk A, Hasenkampf CA, Riggs CD: Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis. Plant J 1997, 12:1261-1271.
  • [12]Beers EP, Jones AM, Dickerman AW: The S8 serine, C1A cysteine and A1 aspartic protease families in Arabidopsis. Phytochemistry 2004, 65:43-58.
  • [13]Rautengarten C, Steinhauser D, Bussis D, Stintzi A, Schaller A, Kopka J, Altmann T: Inferring hypotheses on functional relationships of genes: Analysis of the Arabidopsis thaliana subtilase gene family. PLoS Comput Biol 2005, 1:e40.
  • [14]Tripathi L, Sowdhamini R: Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 2006, 7:200. BioMed Central Full Text
  • [15]Schaller A, Stintzi A, Graff L: Subtilases-versatile tools for protein turnover, plant development, and interactions with the environment. Physiol Plant 2012, 145(1):52-66.
  • [16]Mahon P, Bateman A: The PA domain: A protease-associated domain. Protein Sci 2000, 9:1930-1934.
  • [17]Luo X, Hofmann K: The protease-associated domain: A homology domain associated with multiple classes of proteases. Trends Biochem Sci 2001, 26:147-148.
  • [18]Ottmann C, Rose R, Huttenlocher F, Cedzich A, Hauske P, Kaiser M, Huber R, Schaller A: Structural basis for Ca2 + -independence and activation by homodimerization of tomato subtilase 3. Proc Natl Acad Sci U S A 2009, 106:17223-17228.
  • [19]Zhao C, Johnson BJ, Kositsup B, Beers EP: Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol 2000, 123:1185-1196.
  • [20]Othman R, Nuraziyan A: Fruit-specific expression of papaya subtilase gene. J Plant Physiol 2010, 167(2):131-137.
  • [21]Beilinson V, Moskalenko OV, Livingstone DS, Reverdatto SV, Jung R, Nielsen NC: Two subtilisin-like proteases from soybean. Physiol Plant 2002, 115:585-597.
  • [22]D'Erfurth I, Le Signor C, Aubert G, Sanchez M, Vernoud V, Darchy B, Lherminier J, Bourion V, Bouteiller N, Bendahmane A, Buitink J, Prosperi JM, Thompson R, Burstin J, Gallardo K: A role for an endosperm-localized subtilase in the control of seed size in legumes. New Phytol 2012, 196(3):738-751.
  • [23]Neuteboom LW, Veth-Tello LM, Clijdesdale OR, Hooykaas PJ, van derZaal BJ: A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res 1999, 6:13-19.
  • [24]Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP, Kalinina NO, Taliansky ME, Vartapetian AB: A plant-caspase-like protease activated during hypersensitive response. Plant Cell 2004, 16:157-171.
  • [25]Tian M, Kamoun S: A two disulfide bridge Kazal domain from Phytophthora exhibits stable inhibitory activity against serine proteases of the subtilisin family. BMC Biochem 2005, 6:15. BioMed Central Full Text
  • [26]Tian MY, Benedetti B, Kamoun S: A second kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 2005, 138:1785-1793.
  • [27]Srivastava R, Liu L, Howell SH: Proteolytic processing of a precursor protein for a growth promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 2008, 56:219-227.
  • [28]Coffeen WC, Wolpert TJ: Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 2004, 16:857-873.
  • [29]Vartapetian AB, Tuzhikov AL, Chichkova NV, Taliansky M, Wolpert TJ: A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ 2011, 18:1289-1297.
  • [30]Marchler-Bauer A, Lu SN, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwads M, Hurwitz DI, KE Z, Jackson JD, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang N, Sheng C, Bryant SH: CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39(Database issue):D225-D229.
  • [31]Rose R, Schaller A, Ottmann C: Structural features of plant subtilases. Plant Signal Behav 2010, 5(2):180-183.
  • [32]Emanuelsson O, Nielsen H, Brunak S, von Heijne G: Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016.
  • [33]von Groll U, Berger D, Altmann T: The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 2002, 14:1527-1539.
  • [34]Hamilton JM, Simpson DJ, Hyman SC, Ndimba BK, Slabas AR: Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization. Biochem J 2003, 370(Pt 1):57-67.
  • [35]Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C, Machida Y: A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 2001, 128(23):4681-4689.
  • [36]Jorda L, Coego A, Conejero V, Vera P: A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 1999, 274(4):2360-2365.
  • [37]Meichtry J, Amrhein N, Schaller A: Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol 1999, 39(4):749-760.
  • [38]Tan-Wilson A, Bandak B, Prabu-Jeyabalan M: The PA domain is crucial for determining optimum substrate length for soybean protease C1: Structure and kinetics correlate with molecular function. Plant Physiol Biochem 2012, 53:27-32.
  • [39]Bergeron F, Leduc R, Day R: Subtilase-like pro-protein convertases: from molecular specificity to therapeutic applications. J Mol Endocrinol 2000, 24(1):1-22.
  • [40]Siezen RJ: Subtilases: subtilisin-like serine proteases. Adv Exp Med Biol 1996, 379:75-93.
  • [41]Muszewska A, Taylor JW, Szczesny P, Grynberg M: Independent subtilases expansions in fungi associated with animals. Mol Biol Evol 2011, 28(12):3395-3404.
  • [42]Bailey TL, Williams N, Misleh C, Li WW: MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 2006, 34(Web Server issue):W369-W373.
  • [43]Cao J, Shi F, Liu X, Huang G, Zhou M: Phylogenetic analysis and evolution of aromatic amino acid hydroxylase. FEBS Lett 2010, 584(23):4775-4782.
  • [44]Cao J, Shi F: Dynamics of arginase gene evolution in metazoans. J Biomol Struct Dyn 2012, 30:407-418.
  • [45]Roy SW, Gilbert W: The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 2006, 7(3):211-221.
  • [46]Pearce G, Yamaguchi Y, Barona G, Ryan CA: A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Proc Natl Acad Sci USA 2010, 107(33):14921-14925.
  • [47]Aubourg S, Kreis M, Lecharny A: The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res 1999, 27(2):628-636.
  • [48]Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD: The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci U S A 2002, 99(17):11519-11524.
  • [49]Chen Y, Hao X, Cao J: Small auxin upregulated RNA (SAUR) gene family in maize: Identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. J Integr Plant Biol 2014, 56:133-150.
  • [50]Cao J, Huang J, Yang Y, Hu X: Analyses of the oligopeptide transporter gene family in poplar and grape. BMC Genomics 2011, 12:465. BioMed Central Full Text
  • [51]Chen Y, Cao J: Comparative genomic analysis of the Sm gene family in rice and maize. Gene 2014, 539:238-249.
  • [52]Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, et al.: The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449(7161):463-467.
  • [53]Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, Abe A, Calvo SE, Corrochano LM, Engels R, Fu J, Hansberg W, Kim JM, Kodira CD, Koehrsen MJ, Liu B, Miranda-Saavedra D, O’Leary S, Ortiz-Castellanos L, Poulter R, Rodriguez-Romero J, Ruiz-Herrera J, Shen YQ, Zeng Q, Galagan J, Birren BW, et al.: Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 2009, 5(7):e1000549.
  • [54]Gu X: Maximum-likelihood approach for gene family evolution under functional divergence. Mol Biol Evol 2001, 18(4):453-464.
  • [55]Rawlings ND, Barrett AJ: Families of serine peptidases. Meth Enzymol 1994, 244:19-61.
  • [56]Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21(10):2531-2533.
  • [57]Kosakovsky Pond SLFS: Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005, 22(5):1208-1222.
  • [58]Schaller A, Stintzi A, Graff L: Robust inference of positive selection from recombining coding sequences. Bioinformatics 2006, 22(20):2493-2499.
  • [59]Subbian E, Yabuta Y, Shinde U: Positive selection dictates the choice between kinetic and thermodynamic protein folding and stability in subtilases. Biochemistry 2004, 43(45):14348-14360.
  • [60]Neuteboom LW, Veth-Tello LM, Clijdesdale OR, Hooykaas PJ, van der Zaal BJ: A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res 1999, 6(1):13-19.
  • [61]Budic M, Sabotic J, Meglic V, Kos J, Kidric M: Characterization of two novel subtilases from common bean (Phaseolus vulgaris L.) and their responses to drought. Plant Physiol Biochem 2013, 62:79-87.
  • [62]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
  • [63]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-321.
  • [64]Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO: Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 2006, 6:29. BioMed Central Full Text
  • [65]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28:2731-2739.
  • [66]Gaut BS, Morton BR, McCaig BC, Clegg MT: Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci U S A 1996, 93(19):10274-10279.
  • [67]Delport W, Poon AF, Frost SD, Kosakovsky Pond SL: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26(19):2455-2457.
  • [68]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13(5):555-556.
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