CAREER: Discovering the Developmental Genetic Basis for Parallel Evolution of Aerial Respiration in Arthropods

职业：发现节肢动物空中呼吸平行进化的发育遗传基础

• 批准号: 1552610
• 负责人: Prashant Sharma
• 金额: $ 85万
• 依托单位: University of Wisconsin-Madison
• 依托单位国家: 美国
• 项目类别: Continuing Grant
• 财政年份: 2016
• 资助国家: 美国
• 起止时间: 2016-03-01 至 2022-02-28
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1552610&HistoricalAwards=false
• 关键词: CAREER; Discovering; Developmental; Genetic; Basis

The movement from water to land was a critical evolutionary transformation for both vertebrates and arthropods (insects, spiders, millipedes, crustaceans, etc.). Different groups of arthropods used different methods to enable breathing air, a critical requirement for life on land, a change that occurred separately in at least 7 groups. The goal of this project is to investigate how an air-breathing respiratory system evolved separately in multiple arthropod groups. Did evolution of aerial respiration involve alteration to the same anatomical structures and genes in each group, or does each arthropod group use a different solution to the problem of breathing air? To resolve this question, the embryonic formation of respiratory organs in eight arthropod species will be investigated. Genes and proteins will be tested to determine whether the same genes are used in the respiratory system of all arthropods. Genome sequencing will further test and identify genes that create unique respiratory structures (e.g., the book lung of spiders). The outcomes of this research will be integrated into a new laboratory-based course on invertebrate zoology, to be taught annually through the Department of Zoology, using live specimens. A museum exhibit will be developed on the movement of arthropods onto land, and using evidence from fossils, genes, and developmental biology. One postdoctoral fellow, one graduate student, and ten summer undergraduates will be trained during the work, emphasizing recruitment of women and underrepresented groups in science.Investigating the parallel evolution of aerial respiration in Arthropoda has previously been limited to studies of functional morphology or expression data from a few taxa. Some developmental data suggest that mandibulate and chelicerate respiratory systems are directly homologous, whereas a separate set of data suggests that respiratory organs of arachnids arose independently from modified walking legs. Respiratory systems of Myriapoda have not been studied in a developmental genetic context at all. To resolve the origins of internalized respiratory systems of arthropods, the proposed work will examine positional, genetic, and serial homology of respiratory organs in eight emerging model arthropod systems. To establish the serial homology of arachnid respiratory organs, Hox misexpression experiments will be conducted to derepress appendages in posterior segments. To establish degree of conservation of the gene regulatory network (GRN) underlying tubulogenesis across Arthropoda, gene expression assays will be performed for candidate genes known to be required for establishment of the Drosophila melanogaster tracheal tubule system. To assess functional correspondence, knockdown experiments will be conducted in two chelicerate and three mandibulate exemplars for five critical genes in the Drosphila GRN. To investigate the patterning of the arachnid book lung, comparative transcriptomic data will be generated from book lung primordia of spiders and scorpions, toward identifying a set of novel candidate genes putatively involved in book lung morphogenesis for further functional screening. This work will directly address the two competing scenarios of arthropod terrestrialization that persist in the literature, using independent tests of positional, serial, and genetic homology.

从水到陆地的迁移对脊椎动物和节肢动物（昆虫、蜘蛛、千足虫、甲壳类动物等）来说都是一个关键的进化转变。不同的节肢动物群体使用不同的方法来呼吸空气，这是陆地生命的关键需求，至少有7个群体分别发生了这种变化。这个项目的目标是研究一个呼吸空气的呼吸系统是如何在多个节肢动物群体中分别进化的。空气呼吸的进化是否涉及到每一组动物相同的解剖结构和基因的改变，还是每一组节肢动物使用不同的方法来解决呼吸空气的问题？为了解决这个问题，我们将对8种节肢动物的呼吸器官的胚胎形成进行研究。将对基因和蛋白质进行测试，以确定所有节肢动物的呼吸系统是否使用相同的基因。基因组测序将进一步测试和识别创造独特呼吸结构的基因（例如，蜘蛛的书肺）。这项研究的成果将被整合到一门新的无脊椎动物实验课程中，该课程将通过动物学系每年教授一次，使用活体标本。博物馆将利用化石、基因和发育生物学的证据，展出节肢动物在陆地上的运动。在这项工作中，将培训一名博士后、一名研究生和十名暑期本科生，强调在科学领域招募女性和代表性不足的群体。对节肢动物空中呼吸平行进化的研究以前仅限于对少数类群的功能形态学或表达数据的研究。一些发育数据表明，下颌骨呼吸系统和螯合呼吸系统是直接同源的，而另一组数据表明，蛛形纲动物的呼吸器官是独立于改良的行走腿而产生的。多足类动物的呼吸系统还没有在发育遗传背景下进行过研究。为了解决节肢动物内化呼吸系统的起源，本研究将研究八个新兴节肢动物系统中呼吸器官的位置、遗传和序列同源性。为了建立蛛形动物呼吸器官的序列同源性，我们将进行Hox错表达实验来抑制后节附属物。为了确定节肢动物小管形成的基因调控网络（GRN）的保护程度，将对已知的黑腹果蝇气管小管系统建立所需的候选基因进行基因表达测定。为了评估功能的一致性，我们将在两个螯合体和三个下颌骨样本中对果蝇GRN中的五个关键基因进行敲除实验。为了研究蛛形纲书肺的模式，我们将从蜘蛛和蝎子的书肺原基中获得比较转录组数据，以确定一组新的候选基因，这些基因被认为与书肺形态发生有关，从而进行进一步的功能筛选。这项工作将通过独立的位置、序列和基因同源性测试，直接解决文献中存在的节肢动物陆地化的两种相互竞争的情况。

项目成果

Systemic paralogy and function of retinal determination network homologs in arachnids.

• DOI: 10.1186/s12864-020-07149-x
• 发表时间: 2020-11-23
• 期刊: BMC genomics
• 影响因子: 4.4
• 作者: Gainett G;Ballesteros JA;Kanzler CR;Zehms JT;Zern JM;Aharon S;Gavish-Regev E;Sharma PP
• 通讯作者: Sharma PP

The genome of a daddy-long-legs (Opiliones) illuminates the evolution of arachnid appendages

• DOI: 10.1098/rspb.2021.1168
• 发表时间: 2021-08-11
• 期刊: PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
• 影响因子: 4.7
• 作者: Gainett, Guilherme;Gonzalez, Vanessa L.;Sharma, Prashant P.
• 通讯作者: Sharma, Prashant P.