Boron toxicity is a worldwide problem for crop production, yet we have only a limited understanding of the genetic responses and adaptive mechanisms to this environmental stress in plants. Here we identified responses to excess boron in boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula using comparative genomics, transcriptomics, metabolomics, and ionomics. S. parvula maintains a lower level of total boron and free boric acid in its roots and shoots and sustains growth for longer durations than A. thaliana when grown with excess boron. S. parvula likely excludes boron more efficiently than A. thaliana, which we propose is partly driven by BOR5, a boron transporter that we functionally characterized in the current study. Both species allocate significant transcriptomic and metabolomic resources to enable their cell walls to serve as a partial sink for excess boron, particularly discernable in A. thaliana shoots. We provide evidence that the S. parvula transcriptome is pre-adapted to boron toxicity, exhibiting substantial overlap with the boron-stressed transcriptome of A. thaliana. Our transcriptomic and metabolomics data also suggest that RNA metabolism is a primary target of boron toxicity. Cytoplasmic boric acid likely forms complexes with ribose and ribose-containing compounds critical to RNA and other primary metabolic functions. A model depicting some of the cellular responses that enable a plant to grow in the presence of normally toxic levels of boron is presented.

中文翻译：

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跨物种多组学揭示了细胞壁螯合和升高的全局转录作为植物对硼的耐受性机制

硼的毒性是作物生产的全球性问题，但我们对植物对这种环境胁迫的遗传反应和适应机制的了解还很有限。在这里，我们通过比较基因组学，转录组学，代谢组学和ionomics，确定了对硼胁迫敏感拟南芥及其相对耐硼胁迫的极端微生物中过量硼的响应。当与过量的硼一起生长时，小叶葡萄球菌在其根和茎中保持较低水平的总硼和游离硼酸，并且可以比拟南芥更长的生长持续时间。S. parvula可能比拟南芥更有效地排除硼我们提出的，部分是由BOR5驱动的，BOR5是我们在当前研究中功能上表征的硼转运蛋白。两种物种都分配了大量的转录组和代谢组学资源，以使它们的细胞壁能够作为过量硼的部分吸收池，尤其是在拟南芥芽中可以辨别。我们提供证据表明小叶葡萄球菌转录组是预先适应硼毒性的，与拟南芥的硼胁迫转录组表现出实质性重叠。我们的转录组和代谢组学数据也表明RNA代谢是硼毒性的主要目标。细胞质硼酸可能与核糖和含核糖的化合物形成复合物，这些化合物对RNA和其他主要代谢功能至关重要。提出了描述一些使植物在正常毒性水平的硼下生长的细胞应答的模型。