Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, China.
Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, China; State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; University of Chinese Academy of Sciences, Beijing 100049, China.
Plant Commun. 2024 Jan 8;5(1):100671. doi: 10.1016/j.xplc.2023.100671. Epub 2023 Aug 8.
Plant root-nodule symbiosis (RNS) with mutualistic nitrogen-fixing bacteria is restricted to a single clade of angiosperms, the Nitrogen-Fixing Nodulation Clade (NFNC), and is best understood in the legume family. Nodulating species share many commonalities, explained either by divergence from a common ancestor over 100 million years ago or by convergence following independent origins over that same time period. Regardless, comparative analyses of diverse nodulation syndromes can provide insights into constraints on nodulation-what must be acquired or cannot be lost for a functional symbiosis-and the latitude for variation in the symbiosis. However, much remains to be learned about nodulation, especially outside of legumes. Here, we employed a large-scale phylogenomic analysis across 88 species, complemented by 151 RNA-seq libraries, to elucidate the evolution of RNS. Our phylogenomic analyses further emphasize the uniqueness of the transcription factor NIN as a master regulator of nodulation and identify key mutations that affect its function across the NFNC. Comparative transcriptomic assessment revealed nodule-specific upregulated genes across diverse nodulating plants, while also identifying nodule-specific and nitrogen-response genes. Approximately 70% of symbiosis-related genes are highly conserved in the four representative species, whereas defense-related and host-range restriction genes tend to be lineage specific. Our study also identified over 900 000 conserved non-coding elements (CNEs), over 300 000 of which are unique to sampled NFNC species. NFNC-specific CNEs are enriched with the active H3K9ac mark and are correlated with accessible chromatin regions, thus representing a pool of candidate regulatory elements for genes involved in RNS. Collectively, our results provide novel insights into the evolution of nodulation and lay a foundation for engineering of RNS traits in agriculturally important crops.
植物根瘤共生（RNS）与互利固氮细菌仅限于被子植物的一个单系，即固氮结瘤群（NFNC），在豆科植物中研究得最好。具有结瘤特性的物种有许多共同之处，这些共同点要么是由于 1 亿多年前从共同祖先分化而来，要么是由于在同一时期独立起源而趋同进化而来。无论如何，对不同结瘤综合征的比较分析可以深入了解结瘤的限制因素——对于功能共生，必须获得什么或不能失去什么——以及共生的变化幅度。然而，与豆科植物相比，人们对结瘤的了解还有很多。在这里，我们利用 88 个物种的大规模系统基因组学分析，并辅以 151 个 RNA-seq 文库，阐明了 RNS 的进化。我们的系统基因组学分析进一步强调了转录因子 NIN 的独特性，它是结瘤的主要调节因子，并确定了影响其在 NFNC 中功能的关键突变。比较转录组评估揭示了不同结瘤植物中特定于根瘤的上调基因，同时也鉴定了特定于根瘤和氮响应的基因。在四个代表性物种中，大约 70%的共生相关基因高度保守，而与防御和宿主范围限制相关的基因往往是谱系特异性的。我们的研究还鉴定了超过 90 万个保守的非编码元件（CNEs），其中超过 30 万个是 NFNC 特有物种的。NFNC 特有的 CNEs 富含活跃的 H3K9ac 标记，并与可及染色质区域相关，因此代表了参与 RNS 的基因的候选调节元件池。总的来说，我们的研究结果为结瘤进化提供了新的见解，并为在农业上重要的作物中工程化 RNS 特性奠定了基础。
