Genome Expansion and Differential Expression of Amino Acid Transporters at the Aphid/Buchnera Symbiotic Interface

Genome Expansion and Differential Expression of Amino Acid Transporters at the Aphid/Buchnera Symbiotic Interface
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DOI:
10.1093/molbev/msr140
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发表时间:
2011-11-01
影响因子:
10.7
通讯作者:
Wilson, Alex C. C.
Wilson, Alex C. C.
中科院分区:
生物学1区
文献类型:
--
作者:
Price, Daniel R. G.;Duncan, Rebecca P.;Wilson, Alex C. C.

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在昆虫中,一些生态上最重要的共生体是营养共生体,它们为宿主提供新的性状,从而促进对原本难以进入的生态位的利用。其中一种共生现象是蚜虫与γ-变形菌Buchnera aphidicola的古老的专性细胞内共生。虽然蚜虫/Buchnera共生的营养基础是很好的理解,调解共生伙伴的亲密相互作用的过程和结构仍然没有特点。在这里,使用从头开始的方法,我们的特点是40个氨基酸的多胺有机定位(APC)超家族成员氨基酸转运蛋白(AAT)的基因组中编码的豌豆蚜虫,Acyrthosiphon豌豆的互补。我们发现A.豌豆APC超家族以广泛的基因重复为特征,A.豌豆比其他完全测序的昆虫具有更多的APC超家族转运蛋白,包括APC转运蛋白slimfast的10个副蚜虫特异性扩增。详细的表达分析的基础上选择的17个转运蛋白的系统发育关系,在早期的细菌表达的序列标签研究中确定的5个AAT区分已招募的氨基酸转运在共生界面的细菌细胞的一个子集的8个转运蛋白。这八种转运蛋白包括在细菌细胞中高度表达和/或高度富集的转运蛋白,有趣的是,显示细菌细胞富集表达的四种AAT都是基因家族扩增的成员,而在细菌细胞中高度表达但不富集的四种中的三种与其他基因组中的转运蛋白保持一对一的同源性。最后,分析了大规模A.豌豆Slimfast扩增表明分子进化速率的增加与表达的两个主要变化一致:1)肠表达的丧失和可能的细菌细胞表达的获得,以及2)在无性雌性的所有调查组织中表达的丧失。两者合计,我们的营养AAT在蚜虫/Buchnera共生界面的表征提供了第一次检查的过程和结构的专性细胞内昆虫营养共生的界面上运行,提供独特的见解的类型的基因组变化,可能促进进化的共生维护。
In insects, some of the most ecologically important symbioses are nutritional symbioses that provide hosts with novel traits and thereby facilitate exploitation of otherwise inaccessible niches. One such symbiosis is the ancient obligate intracellular symbiosis of aphids with the gamma-proteobacteria, Buchnera aphidicola. Although the nutritional basis of the aphid/Buchnera symbiosis is well understood, the processes and structures that mediate the intimate interactions of symbiotic partners remain uncharacterized. Here, using a de novo approach, we characterize the complement of 40 amino acid polyamine organocation (APC) superfamily member amino acid transporters (AATs) encoded in the genome of the pea aphid, Acyrthosiphon pisum. We find that the A. pisum APC superfamily is characterized by extensive gene duplications such that A. pisum has more APC superfamily transporters than other fully sequenced insects, including a ten paralog aphid-specific expansion of the APC transporter slimfast. Detailed expression analysis of 17 transporters selected on the basis of their phylogenetic relationship to five AATs identified in an earlier bacteriocyte expressed sequence tag study distinguished a subset of eight transporters that have been recruited for amino acid transport in bacteriocyte cells at the symbiotic interface. These eight transporters include transporters that are highly expressed and/or highly enriched in bacteriocytes and intriguingly, the four AATs that show bacteriocyte-enriched expression are all members of gene family expansions, whereas three of the four that are highly expressed but not enriched in bacteriocytes retain one-to-one orthology with transporters in other genomes. Finally, analysis of evolutionary rates within the large A. pisum slimfast expansion demonstrated increased rates of molecular evolution coinciding with two major shifts in expression: 1) a loss of gut expression and possibly a gain of bacteriocyte expression and 2) loss of expression in all surveyed tissues in asexual females. Taken together, our characterization of nutrient AATs at the aphid/Buchnera symbiotic interface provides the first examination of the processes and structures operating at the interface of an obligate intracellular insect nutritional symbiosis, offering unique insight into the types of genomic change that likely facilitated evolutionary maintenance of the symbiosis.