Genome-wide identification and characterization of WUSCHEL-related homeobox(WOX) genes in Salix suchowensis
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摘要
Members of the WUSCHEL-related homeobox(WOX) transcription factor family are essential for determining cell fate and regulating diverse developmental processes in plants. Many WOX genes have been systematically investigated in woody plants such as Populus trichocarpa, but not in Salix suchowensis. Whole-genome sequence data for S. suchowensis is now available for comprehensive study of WOX genes in S. suchowensis. We thus surveyed the genome of S. suchowensis and demonstrated active expression of 15 WOX genes. In a phylogenetic analysis of WOX genes, the 15 SsWOX genes clustered among the modern/WUS, intermediate and ancient clades similar to the WOX genes of Arabidopsis thaliana. Based on the conserved intron/exon structure,SsWOX genes in the same subgroup had similar conserved exon–intron structures and motif domains. Furthermore,among several Ss WOX subgroups, WUS(Wuschel)-box and EAR(the ERF-associated amphiphilic repression)-like motifs were conserved. Expression profiles of WOX genes in roots, stems and leaves indicate that SsWOX genes have various conserved roles in the tissues. Comparative analysis of the expression patterns in Salix suchowensis with that of Arabidopsis suggests that different shoot regeneration abilities are controlled by different WOX genes in plants. The analysis provide an overview of differentially expressed SsWOX genes during shoot regeneration, but also contribute to understanding the evolution of WOX genes in Salicaceae and the interrelations of WOX genes and other transcription factors, providing targets for further study.
Members of the WUSCHEL-related homeobox(WOX) transcription factor family are essential for determining cell fate and regulating diverse developmental processes in plants. Many WOX genes have been systematically investigated in woody plants such as Populus trichocarpa, but not in Salix suchowensis. Whole-genome sequence data for S. suchowensis is now available for comprehensive study of WOX genes in S. suchowensis. We thus surveyed the genome of S. suchowensis and demonstrated active expression of 15 WOX genes. In a phylogenetic analysis of WOX genes, the 15 SsWOX genes clustered among the modern/WUS, intermediate and ancient clades similar to the WOX genes of Arabidopsis thaliana. Based on the conserved intron/exon structure,SsWOX genes in the same subgroup had similar conserved exon–intron structures and motif domains. Furthermore,among several Ss WOX subgroups, WUS(Wuschel)-box and EAR(the ERF-associated amphiphilic repression)-like motifs were conserved. Expression profiles of WOX genes in roots, stems and leaves indicate that SsWOX genes have various conserved roles in the tissues. Comparative analysis of the expression patterns in Salix suchowensis with that of Arabidopsis suggests that different shoot regeneration abilities are controlled by different WOX genes in plants. The analysis provide an overview of differentially expressed SsWOX genes during shoot regeneration, but also contribute to understanding the evolution of WOX genes in Salicaceae and the interrelations of WOX genes and other transcription factors, providing targets for further study.
Members of the WUSCHEL-related homeobox(WOX) transcription factor family are essential for determining cell fate and regulating diverse developmental processes in plants. Many WOX genes have been systematically investigated in woody plants such as Populus trichocarpa, but not in Salix suchowensis. Whole-genome sequence data for S. suchowensis is now available for comprehensive study of WOX genes in S. suchowensis. We thus surveyed the genome of S. suchowensis and demonstrated active expression of 15 WOX genes. In a phylogenetic analysis of WOX genes, the 15 SsWOX genes clustered among the modern/WUS, intermediate and ancient clades similar to the WOX genes of Arabidopsis thaliana. Based on the conserved intron/exon structure,SsWOX genes in the same subgroup had similar conserved exon–intron structures and motif domains. Furthermore,among several Ss WOX subgroups, WUS(Wuschel)-box and EAR(the ERF-associated amphiphilic repression)-like motifs were conserved. Expression profiles of WOX genes in roots, stems and leaves indicate that SsWOX genes have various conserved roles in the tissues. Comparative analysis of the expression patterns in Salix suchowensis with that of Arabidopsis suggests that different shoot regeneration abilities are controlled by different WOX genes in plants. The analysis provide an overview of differentially expressed SsWOX genes during shoot regeneration, but also contribute to understanding the evolution of WOX genes in Salicaceae and the interrelations of WOX genes and other transcription factors, providing targets for further study.
引文
Bailey TL,Williams N,Misleh C(2006)MEME:discovering and analyzing DNA and protein sequence motifs.Nucleic Acids Res34(Web Server issue):W369
Bi C,Xu Y,Ye Q(2016)Genome-wide identification and characterization of WRKY gene family in Salix suchowensis.Peer J4(9):e2437
Breuninger H et al(2008)Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo.Dev Cell 14(6):867-876
Cao Y,Han Y,Meng D(2017)Genome-wide analysis suggests the relaxed purifying selection affect the evolution of WOX genes in Pyrus bretschneideri,Prunus persica,Prunus mume,and Fragaria vesca.Front Genet 8:78
Dai X,Hu Q,Cai Q(2014)The willow genome and divergent evolution from poplar after the common genome duplication.Cell Res 24(10):1274
Dolzblasz A,Nardmann J,Clerici E(2016)Stem cell regulation by arabidopsis WOX genes.Mol Plant 9(7):1028-1039
Etchells JP,Provost CM,Mishra L(2013)WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation.Development 140(10):2224
Finn RD,Bateman A,Clements J(2016)The Pfam protein families database.Nucleic Acids Res 42(Database issue):D222-230
Gambino G,Minuto M,Boccacci P(2011)Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera.J Exp Bot 62(3):1089
Ge Y,Liu J,Zeng M(2016)Identification of WOX family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes.Front Plant Sci 7(291):93
Graaff EVD,Laux T,Rensing SA(2009)The WUS homeoboxcontaining(WOX)protein family.Genome Biol 10(12):248
Gu Z,Cavalcanti A,Chen FC,Bouman P,Li WH(2002)Extent of gene duplication in the genomes of Drosophila,nematode,and yeast.Mol Biol Evol 19(3):256-262
Haecker A,Grosshardt R,Geiges B(2004)Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana.Development131(3):657-668
Hirakawa Y,Kondo Y,Fukuda H(2010)TDIF peptide signaling regulates vascular stem cell proliferation via the wox4 homeobox gene in Arabidopsis.Plant Cell 22(8):2618-2629
Hu B,Jin J,Guo A(2015)GSDS 2.0:an upgraded gene feature visualization server.Bioinformatics 31(8):1296
Ikeda M,Ohme-Takagi M(2009)Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning.Plant Cell21(11):3493-3505
Ji J,Shimizu R,Sinha N,Scanlon MJ(2010a)Analyses of WOX4transgenics provide further evidence for the evolution of the gene family during the regulation of diverse stem cell functions.Plant Signal Behav 5(7):916-920
Ji J,Strable J,Shimizu R(2010b)WOX4 promotes procambial development.Plant Physiol 152(3):1346-1356
Jin J,Tian F,Yang DC(2017)Plant TFDB 4.0:toward a central hub for transcription factors and regulatory interactions in plants.Nucleic Acids Res 45(Database issue):D1040-D1045
Kumar S,Stecher G,Tamura K(2016)MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol Biol Evol 33(7):1870
Larkin MA,Blackshields G,Brown NP(2007)Clustal W and Clustal X version 2.0.Bioinformatics 23(21):2947-2948
Laux T,Mayer KF,Berger J(1996)The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis.Development 122(1):87
Li H,Durbin R(2009)Fast and accurate short read alignment with Burrows-Wheeler transform.Bioinformatics 25:1754-1760.https://doi.org/10.1093/bioinformatics/btp324
Lian G,Wang Q,Ding Z(2014)Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom.Sci World J 2014(1):534140
Lin H,Niu L,Mc Hale NA(2013)Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants.Proc Natl Acad Sci USA110(1):366
Liu B,Wang L,Zhang J(2014)WUSCHEL-related homeobox genes in Populus tomentosa:diversified expression patterns and a functional similarity in adventitious root formation.BMCGenome 15(1):296
Luan F,Wang X,Shang L(2013)A highly efficient regeneration system for watermelon(Citrullus lanatus thunb.).Pak J Bot45(1):145-150
Oshchepkova EA,Omelyanchuk NA,Savina MS(2017)Systems biology analysis of the WOX5 gene and its functions in the root stem cell niche.Russ J Genet Appl Res 7(4):404-420
Romera-Branchat M,Ripoll JJ,Yanofsky MF(2013)The WOX13homeobox gene promotes replum formation in the Arabidopsis thaliana fruit.Plant J 73(1):37-49
Sarkar AK,Luijten M,Miyashima S(2007)Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers.Nature 446(7137):811
Shimizu R,Ji J,Kelsey E(2009)Tissue specificity and evolution of meristematic WOX3 function.Plant Physiol 149(2):841
Suer S,Agusti J,Sanchez P(2011)WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis.Plant Cell 23(9):3247
Team RC(2004-2016)GUI 1.69.R:R:A language and environment for statistical computing.R Foundation for Statistical Computing,Vienna,Austria
Wang X,Cheng F,Rohlsen D(2018)Organellar genome assembly methods and comparative analysis of horticultural plants.Hortic Res 5(1):3
Yang Z,Gong Q,Qin W(2017)Genome-wide analysis of WOXgenes in upland cotton and their expression pattern under different stresses.BMC Plant Biol 17(1):113
Ye N,Wang X,Li J(2017)Assembly and comparative analysis of complete mitochondiral genome sequence of an economic plant Salix suchowensis.Peer J 5:e3148
Zhang X,Zong J,Liu J(2010)Genome-wide analysis of WOX gene family in rice,sorghum,maize,Arabidopsis and poplar.Bull Bot52(11):1016-1026
Zhang Y,Wu R,Qin G(2011)Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis.J Integr Plant Biol 53(6):493-506
Zhang F,Wang Y,Li G(2014)Stenofolia recruits topless to repress asymmetric LEAVES2 at the leaf margin and promote leaf blade outgrowth in Medicago truncatula.Plant Cell 26(2):650
Zhang N,Huang X,Bao Y(2015)Genome-wide identification and expression profiling of WUSCHEL-related homeobox(WOX)genes during adventitious shoot regeneration of watermelon(Citrullus lanatus).Acta Physiol Plant 37(11):1-12
Bi C,Xu Y,Ye Q(2016)Genome-wide identification and characterization of WRKY gene family in Salix suchowensis.Peer J4(9):e2437
Breuninger H et al(2008)Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo.Dev Cell 14(6):867-876
Cao Y,Han Y,Meng D(2017)Genome-wide analysis suggests the relaxed purifying selection affect the evolution of WOX genes in Pyrus bretschneideri,Prunus persica,Prunus mume,and Fragaria vesca.Front Genet 8:78
Dai X,Hu Q,Cai Q(2014)The willow genome and divergent evolution from poplar after the common genome duplication.Cell Res 24(10):1274
Dolzblasz A,Nardmann J,Clerici E(2016)Stem cell regulation by arabidopsis WOX genes.Mol Plant 9(7):1028-1039
Etchells JP,Provost CM,Mishra L(2013)WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation.Development 140(10):2224
Finn RD,Bateman A,Clements J(2016)The Pfam protein families database.Nucleic Acids Res 42(Database issue):D222-230
Gambino G,Minuto M,Boccacci P(2011)Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera.J Exp Bot 62(3):1089
Ge Y,Liu J,Zeng M(2016)Identification of WOX family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes.Front Plant Sci 7(291):93
Graaff EVD,Laux T,Rensing SA(2009)The WUS homeoboxcontaining(WOX)protein family.Genome Biol 10(12):248
Gu Z,Cavalcanti A,Chen FC,Bouman P,Li WH(2002)Extent of gene duplication in the genomes of Drosophila,nematode,and yeast.Mol Biol Evol 19(3):256-262
Haecker A,Grosshardt R,Geiges B(2004)Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana.Development131(3):657-668
Hirakawa Y,Kondo Y,Fukuda H(2010)TDIF peptide signaling regulates vascular stem cell proliferation via the wox4 homeobox gene in Arabidopsis.Plant Cell 22(8):2618-2629
Hu B,Jin J,Guo A(2015)GSDS 2.0:an upgraded gene feature visualization server.Bioinformatics 31(8):1296
Ikeda M,Ohme-Takagi M(2009)Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning.Plant Cell21(11):3493-3505
Ji J,Shimizu R,Sinha N,Scanlon MJ(2010a)Analyses of WOX4transgenics provide further evidence for the evolution of the gene family during the regulation of diverse stem cell functions.Plant Signal Behav 5(7):916-920
Ji J,Strable J,Shimizu R(2010b)WOX4 promotes procambial development.Plant Physiol 152(3):1346-1356
Jin J,Tian F,Yang DC(2017)Plant TFDB 4.0:toward a central hub for transcription factors and regulatory interactions in plants.Nucleic Acids Res 45(Database issue):D1040-D1045
Kumar S,Stecher G,Tamura K(2016)MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol Biol Evol 33(7):1870
Larkin MA,Blackshields G,Brown NP(2007)Clustal W and Clustal X version 2.0.Bioinformatics 23(21):2947-2948
Laux T,Mayer KF,Berger J(1996)The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis.Development 122(1):87
Li H,Durbin R(2009)Fast and accurate short read alignment with Burrows-Wheeler transform.Bioinformatics 25:1754-1760.https://doi.org/10.1093/bioinformatics/btp324
Lian G,Wang Q,Ding Z(2014)Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom.Sci World J 2014(1):534140
Lin H,Niu L,Mc Hale NA(2013)Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants.Proc Natl Acad Sci USA110(1):366
Liu B,Wang L,Zhang J(2014)WUSCHEL-related homeobox genes in Populus tomentosa:diversified expression patterns and a functional similarity in adventitious root formation.BMCGenome 15(1):296
Luan F,Wang X,Shang L(2013)A highly efficient regeneration system for watermelon(Citrullus lanatus thunb.).Pak J Bot45(1):145-150
Oshchepkova EA,Omelyanchuk NA,Savina MS(2017)Systems biology analysis of the WOX5 gene and its functions in the root stem cell niche.Russ J Genet Appl Res 7(4):404-420
Romera-Branchat M,Ripoll JJ,Yanofsky MF(2013)The WOX13homeobox gene promotes replum formation in the Arabidopsis thaliana fruit.Plant J 73(1):37-49
Sarkar AK,Luijten M,Miyashima S(2007)Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers.Nature 446(7137):811
Shimizu R,Ji J,Kelsey E(2009)Tissue specificity and evolution of meristematic WOX3 function.Plant Physiol 149(2):841
Suer S,Agusti J,Sanchez P(2011)WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis.Plant Cell 23(9):3247
Team RC(2004-2016)GUI 1.69.R:R:A language and environment for statistical computing.R Foundation for Statistical Computing,Vienna,Austria
Wang X,Cheng F,Rohlsen D(2018)Organellar genome assembly methods and comparative analysis of horticultural plants.Hortic Res 5(1):3
Yang Z,Gong Q,Qin W(2017)Genome-wide analysis of WOXgenes in upland cotton and their expression pattern under different stresses.BMC Plant Biol 17(1):113
Ye N,Wang X,Li J(2017)Assembly and comparative analysis of complete mitochondiral genome sequence of an economic plant Salix suchowensis.Peer J 5:e3148
Zhang X,Zong J,Liu J(2010)Genome-wide analysis of WOX gene family in rice,sorghum,maize,Arabidopsis and poplar.Bull Bot52(11):1016-1026
Zhang Y,Wu R,Qin G(2011)Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis.J Integr Plant Biol 53(6):493-506
Zhang F,Wang Y,Li G(2014)Stenofolia recruits topless to repress asymmetric LEAVES2 at the leaf margin and promote leaf blade outgrowth in Medicago truncatula.Plant Cell 26(2):650
Zhang N,Huang X,Bao Y(2015)Genome-wide identification and expression profiling of WUSCHEL-related homeobox(WOX)genes during adventitious shoot regeneration of watermelon(Citrullus lanatus).Acta Physiol Plant 37(11):1-12