H2 supplied via ammonia borane stimulates lateral root branching via phytomelatonin signaling

Abstract

A reliable and stable hydrogen gas (H2) supply will benefit agricultural laboratory and field trials. Here, we assessed ammonia borane (AB), an efficient hydrogen storage material used in the energy industry, and determined its effect on plant physiology and the corresponding mechanism. Through hydroponics and pot experiments, we discovered that AB increases tomato (Solanum lycopersicum) lateral root (LR) branching and this function depended on the increased endogenous H2 level caused by the sustainable H2 supply. In particular, AB might trigger LR primordia initiation. Transgenic tomato and Arabidopsis (Arabidopsis thaliana) expressing hydrogenase1 (CrHYD1) from Chlamydomonas reinhardtii not only accumulated higher en dogenous H2 and phytomelatonin levels but also displayed pronounced LR branching. These endogenous H2 responses achieved by AB or genetic manipulation were sensitive to the pharmacological removal of phytomelatonin, indicating the downstream role of phytomelatonin in endogenous H2 control of LR formation. Consistently, extra H2 supply failed to influence the LR defective phenotypes in phytomelatonin synthetic mutants. Molecular evidence showed that the phytomelatonin-regu lated auxin signaling network and cell-cycle regulation were associated with the AB/H2 control of LR branching. Also, AB and melatonin had little effect on LR branching in the presence of auxin synthetic inhibitors. Collectively, our integrated approaches show that supplying H2 via AB increases LR branching via phytomelatonin signaling. This finding might open the way for ap plying hydrogen storage materials to horticultural production.

Study details

Article type

Original Research

Duration

4 weeks

Dose comparison

Dose-dependent effects of AB and HRW were tested (0.01–100 mg/L for AB; 25%, 50%, 100% saturated HRW). 1 mg/L AB was found optimal for promoting lateral root branching without adverse effects.

Dose-dependent effect

Yes

Outcome

Positive

Findings

Supplying hydrogen via ammonia borane (AB) increases lateral root branching in tomato and Arabidopsis through a mechanism dependent on phytomelatonin signaling, auxin signaling, and cell-cycle regulation. The effect is H2-dependent, and AB provides a more stable and sustained H2 supply than traditional hydrogen-rich water. The beneficial effect is abolished in phytomelatonin synthesis mutants or by pharmacological inhibition of phytomelatonin or auxin synthesis.