Ammonium overaccumulation in senescent leaves as a novel exclusion mechanism to avoid toxicity in photosynthetically active rice leaves

High ammonium concentration is toxic for most plant species, but some rice cultivars are tolerant by mechanisms not understood yet. We tested the hypothesis that NH4+-tolerance could be associated with an exclusion mechanism involving ammonium deposition on the oldest leaves after triggering localized senescence. An ammonium-tolerant cultivar was exposed to increasing ammonium (NH4+) concentrations for two weeks and afterward subjected to 15 mM throughout 4 weeks, to evaluate toxicity and resistance mechanisms. Plants exposed to similar nitrate (NO3−) concentrations were taken as control. In presence of high NH4+ rice displayed similar nitrogen (N) root influx compared to nitrate-supplied roots. In parallel, these plants exhibited a strong impairment in root growth even after exposure to mild NH4+ concentration (3.75 mM). This response was related to increased activity of type III peroxidases, but no evidence for oxidative stress and tissue damages on roots were apparent. Intriguingly, high NH4+-supplied plants displayed a prominent increase in dry mass of senescent oldest leaves, which were 5-fold higher than that observed in nitrate-supplied ones. Ammonium-treatment induced strong NH4+ accumulation on the dead leaf tissues (by 2.8 mmol g-1 DW) representing 75 % of the total-N in this part. This high deposition rate of potentially toxic NH4+ associated with a “self-destruction” strategy should indicate an exclusion mechanism. In contrast, mature leaves presented low NH4+ content, which was associated with no alterations in both CO2 assimilation and photosystem II activity. Our data suggest that rice displays an unusual NH4+ exclusion mechanism by triggering fast and intense senescence on its older leaves. Afterwards, this process is followed by the death of these leaves and deposition of extremely high amounts of this toxic component but preserving younger photosynthetically active tissues.