Proximal and ultimate causes of adaptive lateral gene transfers in land plants

在多细胞生物中，传统认为进化只通过自然选择进行，发生在单个物种基因组中存在的基因突变。最近关于多细胞动物和植物之间的横向基因转移的报道对这一范式提出了挑战。特别是，我们最近表明，横向获得的基因被整合到一些草的基本代谢中，并通过优化一种新的光合途径，即C4光合作用，对其光合机构的适应做出了贡献。这种特性提高了生活在温暖干燥条件下的植物的生产力，如果使用祖先的C3光合途径将其引入作物，包括水稻和小麦，将导致产量增加。阐明C4光合作用基因自然发生适应性转移的机制将为这一努力开辟新的潜在策略。我们目前还不清楚这些基因转移是如何发生的，以及为什么会发生。我们建议通过测序和比较近亲草的基因组来解决这些问题，这些草在光合作用类型和它们拥有的侧向获得基因的数量上有所不同。该项目将利用高通量测序的可用性，使用比较基因组学来解决进化生物学中的一个关键问题。本文将对异teropsis草属中4个关系密切的类群重新生成完整的基因组，其中2个类群属于同一种复合体，但分别使用C3和C4光合作用。将从同一物种复合体中选择另外30个来自不同大陆并具有不同横向获得基因的个体进行重新测序，并将使用de novo组装作为参考进行基因组组装。所有异源芥产生的标记都将在一个系统发育框架内进行分析，该框架将纳入可公开获得的模式草的完整基因组，其中两种与横向转移基因的供体密切相关。所有在统计上与异体多毛属外物种的同类基因更密切相关的异体多毛属基因将被确定为侧向获得基因。研究人员将对它们周围的基因组区域进行调查，以检验有关转移机制的其他假设。最后，将利用关键C4基因的进化史，包括逐渐的C4适应性变化和功能丧失，来推断接受基因转移的植物的光合类型，从而对外来遗传物质的适应性意义有新的认识。这个多方面的项目将确定适应性横向基因转移是如何以及为什么发生在草类中，从而使人们对允许功能性状在远亲物种之间横向传播的条件有了新的认识。此外，这一基础研究项目将通过阐明允许在野外成功转移的条件，对利用C4光合作用改造水稻以养活不断增长的人口的努力产生直接影响。最后，该计划将为使用不同光合作用类型的密切相关的分类群生成第一个基因组，为鉴定精细遗传（特别是调控）变化提供新的和有价值的资源，这些变化允许草类（生态和经济上最重要的植物群体）适应光合作用。

In multicellular organisms, evolution is classically thought to proceed exclusively through natural selection on mutations occurring within genes present in the genome of a single species. This paradigm has been challenged by recent reports of lateral gene transfers among multicellular animals and plants. In particular, we have recently shown that laterally acquired genes were integrated into the basic metabolism of some grasses and contributed to the adaptation of their photosynthetic apparatus through the optimization of a novel photosynthetic pathway, namely C4 photosynthesis. This trait increases the productivity of plants living in warm and dry conditions and would consequently lead to an increase of yield if introduced into crops using the ancestral C3 photosynthetic pathway, including rice and wheat. Elucidating the mechanisms behind naturally occurring adaptive transfers of genes for C4 photosynthesis among grasses would open new potential strategies for this endeavour. We currently do not understand how or why these gene transfers occurred. We propose to tackle these issues by sequencing and comparing the genomes of closely related grasses that differ in their photosynthetic types and in the number of laterally acquired genes they possess. This project will capitalize on the availability of high-throughput sequencing, using comparative genomics to address a key question in evolutionary biology. Complete genomes will be generated de novo for four closely related taxa of the grass genus Alloteropsis, two of which belong to the same species complex but use C3 and C4 photosynthesis, respectively. Thirty additional individuals from the same species complex, sampled from different continents and with different laterally acquired genes, will be selected for re-sequencing, and their genomes will be assembled using the de novo assemblies as a reference. All markers generated for Alloteropsis will be analysed within a phylogenetic framework that will incorporate publicly available complete genomes for model grasses, two of which are closely related to the donors of laterally transferred genes. All Alloteropsis genes that are statistically more closely related to their equivalents in species outside Alloteropsis will be identified as laterally acquired genes. The genomic regions surrounding them will be investigated to test alternative hypotheses about the mechanism responsible for the transfer. Finally, the evolutionary history of key C4 genes, including gradual C4-adaptive changes and loss of function, will be used to infer the photosynthetic type of the plants that received the gene transfers, shedding new light on the adaptive significance of the foreign genetic material incorporated. This multifaceted project will determine how and why adaptive lateral gene transfers occurred in grasses, enabling new understanding of the conditions that allow the lateral spread of functional traits among distantly related species. In addition, this fundamental research project will have a direct impact on the efforts to engineer rice using C4 photosynthesis to feed the growing human population, by elucidating the conditions that allowed successful transfers in the wild. Finally, the proposed project will generate the first genomes for closely related taxa that use different photosynthetic types, providing new and valuable resources for the identification of the fine-scale genetic (especially regulatory) changes that allow photosynthetic adaptation in grasses, the ecologically and economically most important group of plants.