Jasmonic Acid Gradients Reprogram Rice Transcription: Mild Stress Priming to Growth-Defense Balance to Strong Defense...

Jasmonic acid (JA) is a key phytohormone regulating growth and defense. However, the mechanisms by which JA concentration gradients drive rice transcriptional reprogramming remain poorly understood. This study aimed to elucidate how different concentrations of exogenous JA regulate the rice transcriptome and coordinate subsequent physiological transitions.

Fourteen-day-old rice seedlings were treated with 0.02, 0.1, or 0.5 mM exogenous JA. Transcriptomic profiling as well as phenotypic and gene functional analyses were performed to assess genome-wide responses.

A treatment with 0.1 mM JA increased root length by 19.70%, but decreased shoot height in a dose-dependent manner. Additionally, 0.02 mM JA (low concentration) slightly enriched stress-responsive pathways, while 0.1 mM JA (intermediate concentration) primarily regulated organelle development and growth-related processes. By contrast, 0.5 mM JA (high concentration) strongly activated defense and hormone response pathways. Genes associated with growth, stress resistance, and JA responses had distinct concentration-dependent expression patterns. Specifically, the expression of serine/threonine protein kinase genes was correlated with JA levels. The expression of energy metabolism-related genes (e.g., NADH-ubiquinone oxidoreductase and F0F1-ATP synthase genes) increased in response to low-to-intermediate JA concentrations. Moreover, the expression of defense-related genes (cytochrome P450 CYP2 and iron/ascorbate oxidoreductase genes) was induced by low and high JA concentrations. High JA levels also triggered a positive feedback loop involving JA pathway components, including serine/threonine kinases, predicted E3 ubiquitin ligases, SCP domain-containing defense proteins, chitinases, and MYB transcription factors, thereby amplifying defense signaling.

We developed a concentration-dependent model, where in a JA concentration gradient reprograms the rice transcriptome to drive a sequential physiological transition from mild stress priming through growth-defense balance to robust defense activation. This study provides a mechanistic framework for elucidating how JA mediates growth-defense trade-offs, with possible implications for exploiting exogenous JA during rice cultivation.