Rice plants respond to ammonium stress by adopting a helical root growth pattern

Abstract

High levels of ammonium nutrition reduce plant growth and different plant species have developed distinct strategies to maximize ammonium acquisition while alleviating ammonium toxicity through modulating root growth. To date, the mechanisms underlying plant tolerance or sensitivity towards ammonium remain unclear. Rice (Oryza sativa) uses ammonium as its main N source. Here we show that ammonium supply restricts rice root elongation and induces a helical growth pattern, which is attributed to root acidification resulting from ammonium uptake. Ammonium-induced low pH triggers the asymmetric distribution of auxin in rice root tips through changes in auxin signaling, thereby inducing a helical growth response. Blocking auxin signaling completely inhibited this root response. In contrast, this root response is not activated in ammonium-treated Arabidopsis. Acidification of Arabidopsis roots leads to the protonation of indole-3-acetic acid and dampening of the intracellular auxin signaling levels that are required for maintaining root growth. Our study suggests a different mode of action by ammonium on the root pattern and auxin response machinery in rice versus Arabidopsis, and the rice-specific helical root response towards ammonium is an expression of the ability of rice to moderate auxin signaling and root growth to utilize ammonium while confronting acidic stress.

Ammonium regulates the development of pine roots through hormonal crosstalk and differential expression of transcription factors in the apex

“…These results suggest that NH 4 + triggers an alteration in polar auxin transport (PAT) involving a highly coordinated transcriptomic response between tissues of the pine root. The Nano-PALDI-MSI data confirmed that under a supply of NH 4 + , PAT was impaired, thus promoting a putative local increase in IAA presumably in RC and/or RM tissues where cambial development takes place based on IAA-related transcripts and TF expression (Figures 5A and 7), which could suggest a different regulatory mechanism of those pH-dependent described in rice and Arabidopsis (Jia et al, 2020; Meier et al, 2020). One possible alternative for this PAT alteration could be IAA conjugation with sugars/amino acids as previously described (Tamura et al, 2010; Di et al, 2021).…”

“…The expression of genes coding for PIN transporters was not affected in pine roots. Recently, it has been linked IAA signaling pathway to acidification (Jia et al, 2020; Meier et al, 2020).…”

“…When the quadruple ammonium transporter (AMT) knockout lines, that exhibit a severe reduction in LR branching, were complemented with AtAMT1.1 or AtAMT1.3 , only AtAMT1.3 -complemented plants were able to restore the LR branching phenotype induced by NH 4 + (Lima et al, 2010), suggesting that the NH 4 + -induced LR branching signaling events are dependent on AtAMT1.3 (Lima et al, 2010). Recently, it has been demonstrated that under NH 4 + supply, RSA changes mediated by IAAs transport are highly linked to root acidification (Jia et al, 2020; Meier et al, 2020), which seems to be the molecular basis for the AMT transporter effect on LR branching since NH 4 + uptake is accompanied by pH imbalance. In addition, IAAs have been suggested to be involved in this signaling event due to the repression of PIN2 under a supply of NH 4 + (Y.…”

Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (Oryza sativa L.)

“…Moreover, the helical root phenotype was induced after treatment with >2.5 mM NH 4 NO 3 in the agar medium; this was a sign for ammonium-induced low acidification responses in Nipponbare [ 55 ]. Helical root phenotype was also observed after 1N treatment in LY9348, but not after the other two higher N treatments, 2N and 4N ( Figure 1 A).…”

Physiological and Multi-Omics Approaches for Explaining Drought Stress Tolerance and Supporting Sustainable Production of Rice

“…These attributes helped rice plants to develop tolerance to drought through absorption of water from deep layers of soil (Gowda et al, 2011;Uga et al, 2013a). Moreover, supplementation of rice seedlings with NH 4+ resulted in higher root growth and an increased number of root tips to enhance water uptake under water stress conditions (Jia et al, 2020). In addition, rice seedlings supplemented with NO 3− induced restriction in water uptake resulted in the induction of root aerenchyma formation (Yang et al, 2012).…”