Evolutionary Dynamics of the wnt Gene Family: A Lophotrochozoan Perspective

Evolutionary Dynamics of the wnt Gene Family: A Lophotrochozoan Perspective
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DOI:
10.1093/molbev/msq052
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发表时间:
2010-07-01
影响因子:
10.7
通讯作者:
Weisblat, David A.
Weisblat, David A.
中科院分区:
生物学1区
文献类型:
--
作者:
Cho, Sung-Jin;Valles, Yvonne;Weisblat, David A.

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WNT基因家族编码一组分泌的糖蛋白,参与关键的发育过程,包括细胞命运的指定和后天生长的调节(Cadigan Km,Nusse R.1997)。WNT信号:动物发育中的一个共同主题。吉尼斯·德夫(Gene Dev.)11:3286-3305;Martin BL,Kimelman D.2009。WNT信号与胚胎后期发育的进化。Curr Biol.19:R215-R219)。至于许多其他基因家族,WNT家族的扩张和/或收缩的证据可以从后口动物(例如棘皮动物和脊椎动物[Nusse R,Varmus HE.1992年。WNT基因。牢房。69:1073-1087;舒伯特·M,荷兰LZ,荷兰ND,雅各布斯DK。2000年。基于所有可用的全长序列的Wnt基因的系统发育树,其中包括五个来自文昌鱼的全长序列。摩尔·比奥尔·埃沃。17:1896年-1903年;克罗齐JC,吴思,拜鲁姆C,徐荣,杜洛昆,L,维克拉玛纳亚克啊,盖奇C,麦克雷博士2006。紫球海胆进化上保守的Wnt通路的全基因组调查。戴夫·比奥。300:121-131。])和蜕皮虫(例如节肢动物和线虫[Eisenmann DM.2005年。WNT信令。蠕虫书。1-17;博洛内西R,法尔扎纳L,费舍尔·TD,布朗·斯。2008年。在赤霉菌的短胚胚中,需要多个Wnt基因来进行分割。Curr Biol.18:1624-1629.]),但对第三个主要的双边类群--软体动物和环节动物(例如软体动物和环节动物[Prud‘homme B,Lartillot N,Balvoine G,Adoutte A,Vervoort M.2002.]却知之甚少。Wnt基因家族的系统发育分析。来自Lophotrochozoan成员的见解。Curr Biol.12:1395。]))。为了更全面地了解这个基因家族的进化动态,我们从一个软体动物(Lottia Gigantea)和两个环节动物(Capitella teleta和Helobdella robusta)的全基因组组合中详尽地挖掘了WNT基因序列,并通过系统发育、遗传连锁、内含子-外显子结构和胚胎表达分析对它们进行了分析。获得的36个WNT基因分别代表Lottia、Capitella和Helobdella中的11个、12个和9个不同的WNT亚家族。因此,三个被分析的后生动物基因组中有两个保留了几乎完整的WNT基因的祖先补充,强调了这个基因家族在后生动物中的重要性和复杂性。根据基因复制和丢失、分支长度和遗传连锁的变化判断,水蚤Helobdella的基因组比Lottia和Capitella的基因组反映了更多的活力。最后,我们对Helobdella WNT基因在胚胎发育过程中的表达进行了详细的分析。我们发现,尽管这些模式在早期卵裂阶段显示出相当大的重叠,但每个WNT基因在生发板和组织形态发生期间都有独特的表达模式。将Helobdella中复制的WNT基因与其在Capitella中的同源基因的胚胎表达模式进行比较,发现复制的水蚤WNT基因具有广泛的调控多样性。
The wnt gene family encodes a set of secreted glycoproteins involved in key developmental processes, including cell fate specification and regulation of posterior growth (Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286-3305.; Martin BL, Kimelman D. 2009. Wnt signaling and the evolution of embryonic posterior development. Curr Biol. 19:R215-R219.). As for many other gene families, evidence for expansion and/or contraction of the wnt family is available from deuterostomes (e.g., echinoderms and vertebrates [Nusse R, Varmus HE. 1992. Wnt genes. Cell. 69:1073-1087.; Schubert M, Holland LZ, Holland ND, Jacobs DK. 2000. A phylogenetic tree of the Wnt genes based on all available full-length sequences, including five from the cephalochordate amphioxus. Mol Biol Evol. 17:1896-1903.; Croce JC, Wu SY, Byrum C, Xu R, Duloquin L, Wikramanayake AH, Gache C, McClay DR. 2006. A genome-wide survey of the evolutionarily conserved Wnt pathways in the sea urchin Strongylocentrotus purpuratus. Dev Biol. 300:121-131.]) and ecdysozoans (e.g., arthropods and nematodes [Eisenmann DM. 2005. Wnt signaling. Worm Book. 1-17.; Bolognesi R, Farzana L, Fischer TD, Brown Si. 2008. Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol. 18:1624-1629.]), but little is known from the third major bilaterian group, the lophotrochozoans (e.g., mollusks and annelids [Prud'homme B, Lartillot N, Balavoine G, Adoutte A, Vervoort M. 2002. Phylogenetic analysis of the Wnt gene family. Insights from lophotrochozoan members. Curr Biol. 12:1395.]). To obtain a more comprehensive scenario of the evolutionary dynamics of this gene family, we exhaustively mined wnt gene sequences from the whole genome assemblies of a mollusk (Lottia gigantea) and two annelids (Capitella teleta and Helobdella robusta) and examined them by phylogenetic, genetic linkage, intron-exon structure, and embryonic expression analyses. The 36 wnt genes obtained represent 11, 12, and 9 distinct wnt subfamilies in Lottia, Capitella, and Helobdella, respectively. Thus, two of the three analyzed lophotrochozoan genomes retained an almost complete ancestral complement of wnt genes emphasizing the importance and complexity of this gene family across metazoans. The genome of the leech Helobdella reflects significantly more dynamism than those of Lottia and Capitella, as judged by gene duplications and losses, branch length, and changes in genetic linkage. Finally, we performed a detailed expression analysis for all the Helobdella wnt genes during embryonic development. We find that, although the patterns show substantial overlap during early cleavage stages, each wnt gene has a unique expression pattern in the germinal plate and during tissue morphogenesis. Comparisons of the embryonic expression patterns of the duplicated wnt genes in Helobdella with their orthologs in Capitella reveal extensive regulatory diversification of the duplicated leech wnt genes.