The alleviation of manganese toxicity by ammonium in sugarcane is related to pectin content, pectin methyl esterification, and nitric oxide

Abstract

Coexistence of ammonium (NH4+) with manganese (Mn) in acid soils may facilitate the alleviation of Mn toxicity to plants. However, the effect of NH4+ on Mn toxicity and the corresponding mechanisms are unclear. In this study, the effects of NH4+ and nitrate (NO3‐) on Mn toxicity, cell wall properties, and nitric oxide (NO) signaling in sugarcane were compared. NH4+ alleviated Mn‐induced chlorosis in sugarcane seedlings and increased seedling biomass compared with NO3‐. Exogenous application of NH4+ decreased the root cell wall pectin content and methyl esterase (PME) activity, but increased the degree of root pectin esterification (PMD). These changes were accompanied by reductions in the Mn content in roots, leaves, root cell wall, and cell wall pectin. An analysis of adsorption kinetic revealed less Mn‐adsorption capacity in cell walls extracted from NH4+‐fed than from NO3‐‐fed sugarcane. Mn induced NO accumulation in sugarcane roots, but NH4+‐fed seedlings accumulated less NO. Exogenous application of the NO donor sodium nitroprusside increased the Mn content of root cell wall pectin in NH4+‐fed sugarcane, while the NO scavenger 2‐(4‐carboxyphenyl)‐4,4,5,5‐tetramethylimidazoline‐1‐oxyl‐3‐oxid decreased the Mn content in NO3‐‐fed sugarcane. These treatments eliminated the difference in the pectin Mn content between NH4+‐fed and NO3‐‐fed sugarcane, as did a similar treatment with the nitrate reductase inhibitor tungstate, which decreased root cell wall pectin content and NO accumulation. These results suggest that (i) NH4+ alleviates Mn toxicity in sugarcane by reducing root pectin accumulation and root cell wall PME activity, thereby increasing cell wall PMD and decreasing both the Mn‐binding capacity of cell wall and Mn accumulation, and (ii) NO mediates the accumulation of both pectin and Mn in response to different forms of nitrogen. The physiological mechanisms underlying the alleviation of ammonium on Mn phytotoxicity were clarified, which provided important implication for agricultural production and ecosystem functioning in acid soil.

Changes in the Microbiome of Sugarcane (Saccharum spp. Hybrids.) Rhizosphere in Response to Manganese Toxicity

“…This may indicate there was a significantly increased in rhizosphere bacterial relative functions. Moreover, the relative abundance of proteins related to the conversion of nitrate nitrogen to ammonium nitrogen also significantly increased in the rhizosphere soil, and previous studies have found that ammonium nitrogen is beneficial for the alleviation of Mn toxicity in sugarcane [46]. In conjunction with the WS-Mn and EX-Mn concentration in the rhizosphere soil and bacterial Mn removal ability, this indicated that the activity of these proteins is beneficial for microorganisms to adapt to Mn stress and reduce the availability of Mn 2+ .…”

Manganese and phosphorus maize shoot concentrations are differently affected by nitrification inhibitor‐driven rhizosphere acidification

“…Furthermore, Ling et al. (2022) indicated that the reduced Mn accumulation in sugarcane occurred because of the decreased Mn 2+ ‐binding capacity of the cell wall in NH 4 + ‐fed plants. However, further information about the exact mechanism by which NH 4 + ‐N nutrition reduces Mn 2+ uptake is still scarce in the literature.…”

“…ns, * and ** represent non-significant, significant at p ≤ .05 and significant at p ≤ .01 differences between −DMPP and + DMPP within the same lime rate according to the analysis of variance, F test.such effects,Hu et al (2019) suggested that the rhizosphere acidification caused by NH 4 + -N nutrition resulted in the down-regulation of the OsNramp5 Mn 2+ transporter gene in rice. Furthermore,Ling et al (2022) indicated that the reduced Mn accumulation in sugarcane occurred because of the decreased Mn 2+ -binding capacity of the cell wall in NH 4 + -fed plants. However, further information about the exact mechanism by which NH 4 + -N nutrition reduces Mn 2+ uptake is still scarce in the literature.…”