Requirement of Trichome Formation for the Growth-promoting Effects of Olivine for Enhanced Weathering in Arabidopsis thaliana

Abstract Enhanced rock weathering helps remove CO 2 from air and cools the Earth over geological time periods, while also promoting plant growth, but the molecular mechanism underlying enhanced plant growth is unclear. In this study, ionome and transcriptome analyses revealed the importance of trichome formation for the growth-promoting effects of olivine ground to enhance weathering. In Arabidopsis, the application of 10% (w/w) olivine improved plant growth (a 64.2% increase in leaf area) and caused a 24.7% increase in Mg accumulation determined by ICP-AES at 23 days after germination (DAG) under long-day (16 h light/8 h dark cycle) conditions. Elemental maps of olivine-treated plants at 10 DAG produced by micro-particle-induced x-ray emission showed that olivine significantly altered Mg, K, and S accumulation in trichomes on true leaves, suggesting that trichomes may be critical for olivine-induced growth. The growth of glabrous1 ( gl1-1 and gl1-4 ) mutants defective in trichome initiation was not promoted by olivine. A transcriptome analysis of shoots by RNA-seq from wild-type plants at 16 DAG indicated olivine suppressed biotic stress-responsive gene expression. Additionally, Zn homeostasis was disrupted by olivine in gl1 mutants, implying that decreased Zn availability may inhibit the positive effect of olivine on growth. Collectively, our data uncovered the importance of trichomes to the adaptation of plants to soils containing rock-powders for crop improvement and agricultural sustainability and suggest the possibility that applying olivine might modulate the growth–defense trade-off governed by ion homeostasis mediated through trichome development, leading to improved plant growth.