Evolutionary origin of cAMP-based chemoattraction in the social amoebae

Evolutionary origin of cAMP-based chemoattraction in the social amoebae
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DOI:
10.1073/pnas.0502238102
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发表时间:
2005-05-03
影响因子:
11.1
通讯作者:
Schaap, P
Schaap, P
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Alvarez-Curto, E;Rozen, DE;Schaap, P

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如果整合的发育途径在新的发育阶段表达,然后被招募来服务新的功能,就会出现表型新颖性。我们分析了盘基网柄虫阿米巴新发育特征的起源:cAMP 作为发育化学引诱剂的进化。我们表明,cAMP 吸引饥饿变形虫的作用是通过募集一条最初进化来协调子实体形态发生的途径而产生的,高亲和力 cAMP 受体 (cAR) 的直系同源物 cAR1 在跨越盘基网柄菌系统发育的一系列物种中被鉴定出来。来自基础物种微小盘基网柄菌的 cAR1 直系同源物在缺乏高亲和力 cAR 的衍生物种盘基网柄菌的聚集缺陷突变体中表达时恢复了聚集和发育,从而证明了微小盘基网柄菌 cAR 是一种功能齐全的 cAR。来自基础物种的 cAR1 直向同源物在子实体形成过程中表达,并且只有这个过程(而不是聚集)因 cAR1 功能的废除而被破坏。这与衍生物种相反,衍生物种中 cAR1 也在聚集过程中表达,并严格调节这一过程。我们的数据表明,子实体形成的协调是细胞外 cAMP 信号传导的祖先功能,而其在聚集中的衍生作用是通过将预先存在的途径招募到早期发育阶段而进化的。这很可能是通过向现有的 cAMP 信号基因添加远端顺式调节区域而发生的。
Phenotypic novelties can arise if integrated developmental pathways are expressed at new developmental stages and then recruited to serve new functions. We analyze the origin of a novel developmental trait of Dictyostelid amoebae: the evolution of cAMP as a developmental chemoattractant. We show that cAMP's role of attracting starving amoebae arose through recruitment of a pathway that originally evolved to coordinate fruiting body morphogenesis, Orthologues of the high-affinity cAMP receptor (cAR), cAR1, were identified in a selection of species that span the Dictyostelid phylogeny. The cAR1 orthologue from the basal species Dictyostelium minutum restored aggregation and development when expressed in an aggregation-defective mutant of the derived species Dictyostelium discoideum that lacks high-affinity cARs, thus demonstrating that the D. minutum cAR is a fully functional cAR. cAR1 orthologues from basal species are expressed during fruiting body formation, and only this process, and not aggregation, was disrupted by abrogation of cAR1 function. This is in contrast to derived species, where cAR1 is also expressed during aggregation and critically regulates this process. Our data show that coordination of fruiting body formation is the ancestral function of extracellular cAMP signaling, whereas its derived role in aggregation evolved by recruitment of a preexisting pathway to an earlier stage of development. This most likely occurred by addition of distal cis-regulatory regions to existing cAMP signaling genes.