Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis
Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis
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DOI：
10.1126/science.aat1743
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发表时间：
2018-07-13
期刊：
影响因子：
56.9
通讯作者：
Cheng, Shifeng
中科院分区：
文献类型：
--
作者：
Griesmann, Maximilian;Chang, Yue;Cheng, Shifeng
植物生长需要氮等营养物质。豆科植物和另外九个植物家族受益于固氮根瘤（NFN）共生，其中根形成细胞内宿主固氮细菌的根瘤。在这种互利的共生关系中，细菌将大气中的氮转化为铵，并将其输送到宿主植物。因此，NFN共生使植物能够在陆地生态系统中的氮限制条件下生存。在农业中，这种共生减少了对氮肥的依赖，从而降低了成本，生态影响，以及伴随着大规模施用化肥的化石燃料消耗。RATIONALE分子生物学表明，NFN共生仅限于四个被子植物目--蚕豆目，壳斗目，葫芦目和蔷薇目--它们共同形成了单系NFN分支。然而，只有10的28个植物科在这个分支包含从事NFN共生的物种。即使在这10个科中，大多数属也没有形成这种共生关系。NFN共生需要30多个必需基因的协调功能。这种共生关系在相关的家庭中的存在表明，在NFN分支的祖先的遗传变化，使NFN共生在这个分支的进化。分散分布的功能NFN共生在整个进化枝导致的问题，是否NFN共生进化多次独立的收敛的方式或失去了多次，无论它出现的次数。化石数据一直无法回答这个问题。在这里，我们用分子证据来询问目前的模式与NFN共生的植物物种的演变。我们测序了七个共生物种的基因组，这些物种属于壳斗目，蔷薇目，葫芦目和豆科云实亚科。我们补充了这个数据集的测序三个nonacetulating物种的葫芦目和豆科亚科Cercidoideae和Papilionoideae的基因组。使用全基因组的NFN基因组的方法，我们发现，所有的豆科植物基因与NFN共生的特点是保守的物种有一个例外。我们观察到大量的订单特定的基因家族的扩展，仅仅是因为它们的系统发育分布，可能包括基因有助于多个收益或随后的共生细化。与此同时，我们发现了多个独立的功能丧失事件的基因编码的不可或缺的NFN共生regulatorNONINCEPTION（NIN）的NFN分支内的13个非共生物种的基因组中的10个的签名。该模式表明，至少有8个独立的损失NFN共生。CONCLUSION我们发现，多个独立的损失NFN共生发生在四个订单的NFN分支。这些结果表明，NFN共生以前已经比目前明显的更常见，这种共生是受到低估的不利选择pressure.Phylogenomics和进化的NFN symbioisGenome测序结合27个以前可用的基因组，导致在一个数据集跨越的NFN分支和物种以外的NFN分支作为一个外群的nfnulating和nonnfnulating物种。根据三种系统发育模式鉴定和筛选了两个类群。这个全基因组分析确定了两个参与NFN共生的基因，NIN和根瘤菌导向的极性生长（RPG），这两个基因在大多数非共生物种中丢失。NFN共生体的多重损失（红叉）的发生......
INTRODUCTIONAccess to nutrients such as nitrogen is required for plant growth. Legumes and nine additional plant families benefit from the nitrogen-fixing root nodule (NFN) symbiosis, in which roots develop nodules that intracellularly host nitrogen-fixing bacteria. In this mutually beneficial symbiosis, the bacteria convert atmospheric nitrogen into ammonium and deliver it to the host plant. NFN symbiosis thus enables plant survival under nitrogen-limiting conditions in terrestrial ecosystems. In agriculture, this symbiosis reduces reliance on nitrogen fertilizer, thus reducing the costs, ecological impact, and fossil fuel consumption attendant on large-scale application of fertilizers.RATIONALEMolecular phylogenies show that NFN symbiosis is restricted to four angiosperm orders—Fabales, Fagales, Cucurbitales, and Rosales—that together form the monophyletic NFN clade. However, only 10 of the 28 plant families within this clade contain species engaged in the NFN symbiosis. Even within these 10 families, most genera do not form this symbiosis. The NFN symbiosis requires the coordinated function of more than 30 essential genes. Presence of this symbiosis in related families suggests that a genetic change in the ancestor of the NFN clade enabled evolution of NFN symbiosis in this clade. The scattered distribution of functional NFN symbiosis across the clade has led to the question of whether NFN symbiosis evolved multiple times independently in a convergent manner or was lost multiple times regardless of the number of times it arose. Fossil data have been unable to answer this question. Here we used molecular evidence to ask how the current pattern of plant species with NFN symbiosis evolved.RESULTSWe sequenced the genomes of seven nodulating species belonging to the Fagales, Rosales, and Cucurbitales orders and the legume subfamily Caesalpinioideae. We complemented this dataset by sequencing three genomes of nonnodulating species from the Cucurbitales and from the legume subfamilies Cercidoideae and Papilionoideae. Using a genome-wide phylogenomic approach, we found that all legume genes with a characterized role in NFN symbiosis are conserved in nodulating species with one exception. We observed larger numbers of order-specific gene family expansions that, solely because of their phylogenetic distribution, may include genes contributing to multiple gains or subsequent refinements of the symbiosis. In parallel, we discovered signatures of multiple independent loss-of-function events for the gene encoding the indispensable NFN symbiosis regulatorNODULE INCEPTION(NIN) in 10 of 13 genomes of nonnodulating species within the NFN clade. The pattern suggests at least eight independent losses of NFN symbiosis.CONCLUSIONWe found that multiple independent losses of NFN symbiosis occurred in the four orders of the NFN clade. These results suggest that NFN symbiosis has previously been more common than currently evident and that this symbiosis is subject to an underestimated adverse selection pressure.Phylogenomics and evolution of NFN symbiosisGenome sequencing of nodulating and nonnodulating species combined with 27 previously available genomes resulted in a dataset spanning the NFN clade and species outside the NFN clade as an outgroup. Orthogroups were identified and filtered following three phylogenetic patterns. This genome-wide analysis identified two genes involved in NFN symbiosis,NINandRHIZOBIUM-DIRECTED POLAR GROWTH(RPG), that were lost in most nonnodulating species. The occurrence of multiple losses (red crosses) of NFN symbiosis …