Multi-omics analysis reveals activation of jasmonate synthesis and modulation of oxidative stress responses in boron deficient pea shoots

Boron (B) is vital for plant growth and development. Understanding aboveground tissue responses to B deficiency can offer insights into enhancing plant productivity under B-limited conditions. Here we show from comprehensive metabolomics analysis that during B deficiency treatment the number of differentially expressed metabolites (DEMs) increases from 64 to 193 in pea shoots. Boron deficiency intensified oxidative stress and led to decreased ascorbate and glutathione levels. Integrative metabolomic and transcriptomic analyses revealed activation of the phenylpropanoid biosynthesis and alpha-linolenic acid metabolic pathways under B deficiency. Metabolites of the phenylpropanoid pathway, including p-coumaryl alcohol and sinapic acid, increased, accompanied by upregulation of related biosynthetic genes. A decline in total flavonoid content suggested that the activation of phenylpropanoid synthesis might indicate increased lignin accumulation, thus affecting cell wall metabolism. The alterations in these pathways at specific time point highlighted the dynamic resource allocation caused by B deficiency, providing insights into metabolic reprogramming in pea shoot apices. In the alpha-linolenic acid pathway, B deficiency led to accumulation of 17-hydroxylinolenic acid, jasmonic acid (JA), and jasmonoyl-L-isoleucine, with upregulated JA biosynthesis genes. Jasmonates are proposed to play a key role in reprogramming shoot development particularly modulating membrane and cell wall structure and function under B deficiency. Increased levels of oxidation products of linoleic acid suggest changes to membrane structure and are also consistent with changes to the redox status of cells under B deficiency. Collectively, our findings elucidated intricate B deficiency responses at both the metabolome and transcriptome levels and identified potential targets for breeding crops tolerant to B deficiency, including jasmonate signalling, phenylpropanoid biosynthesis, and antioxidant capacity.