Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Abstract

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.