Wisconsin Institute for Discovery, University of Wisconsin, Madison, WI, 53715, USA.
School of Forest Resources and Conservation, University of Florida, Gainesville, FL, 32611, USA.
BMC Biol. 2022 Nov 9;20(1):252. doi: 10.1186/s12915-022-01450-9.
Symbiotic associations between bacteria and leguminous plants lead to the formation of root nodules that fix nitrogen needed for sustainable agricultural systems. Symbiosis triggers extensive genome and transcriptome remodeling in the plant, yet an integrated understanding of the extent of chromatin changes and transcriptional networks that functionally regulate gene expression associated with symbiosis remains poorly understood. In particular, analyses of early temporal events driving this symbiosis have only captured correlative relationships between regulators and targets at mRNA level. Here, we characterize changes in transcriptome and chromatin accessibility in the model legume Medicago truncatula, in response to rhizobial signals that trigger the formation of root nodules.
We profiled the temporal chromatin accessibility (ATAC-seq) and transcriptome (RNA-seq) dynamics of M. truncatula roots treated with bacterial small molecules called lipo-chitooligosaccharides that trigger host symbiotic pathways of nodule development. Using a novel approach, dynamic regulatory module networks, we integrated ATAC-seq and RNA-seq time courses to predict cis-regulatory elements and transcription factors that most significantly contribute to transcriptomic changes associated with symbiosis. Regulators involved in auxin (IAA4-5, SHY2), ethylene (EIN3, ERF1), and abscisic acid (ABI5) hormone response, as well as histone and DNA methylation (IBM1), emerged among those most predictive of transcriptome dynamics. RNAi-based knockdown of EIN3 and ERF1 reduced nodule number in M. truncatula validating the role of these predicted regulators in symbiosis between legumes and rhizobia.
Our transcriptomic and chromatin accessibility datasets provide a valuable resource to understand the gene regulatory programs controlling the early stages of the dynamic process of symbiosis. The regulators identified provide potential targets for future experimental validation, and the engineering of nodulation in species is unable to establish that symbiosis naturally.
细菌与豆科植物之间的共生关系导致根瘤的形成，根瘤能够固定可持续农业系统所需的氮。共生在植物中引发广泛的基因组和转录组重塑，但对于与共生相关的染色质变化和转录调控网络的功能调控程度的综合理解仍知之甚少。特别是，对驱动这种共生的早期时间事件的分析仅在 mRNA 水平上捕捉到了调控因子与靶基因之间的相关性。在这里，我们研究了模式豆科植物蒺藜苜蓿对根瘤菌信号的反应中，转录组和染色质可及性的变化，这些信号触发根瘤的形成。
我们对用细菌小分子（称为脂寡糖）处理的蒺藜苜蓿根进行了转录组（RNA-seq）和染色质可及性（ATAC-seq）的时间动态分析，这些小分子触发宿主共生途径的结瘤发育。我们使用一种新的方法，动态调控模块网络，将 ATAC-seq 和 RNA-seq 时间过程整合在一起，以预测与共生相关的转录组变化中最重要的顺式调控元件和转录因子。涉及生长素（IAA4-5、SHY2）、乙烯（EIN3、ERF1）和脱落酸（ABI5）激素反应，以及组蛋白和 DNA 甲基化（IBM1）的调节剂，是与转录组动态最相关的调节剂之一。EIN3 和 ERF1 的 RNAi 敲低减少了蒺藜苜蓿的根瘤数量，验证了这些预测的调节剂在豆科植物与根瘤菌共生中的作用。
我们的转录组和染色质可及性数据集为理解控制共生动态过程早期阶段的基因调控程序提供了有价值的资源。鉴定出的调节剂为未来的实验验证提供了潜在的目标，而在不能自然建立共生的物种中，对结瘤的工程设计提供了潜在的目标。
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