Nitric Oxide Acts Downstream of Auxin to Trigger Root Ferric-Chelate Reductase Activity in Response to Iron Deficiency in Arabidopsis      

Abstract

In response to iron (Fe) deficiency, dicots employ a reduction-based mechanism by inducing ferric-chelate reductase (FCR) at the root plasma membrane to enhance Fe uptake. However, the signal pathway leading to FCR induction is still unclear. Here, we found that the Fe-deficiency-induced increase of auxin and nitric oxide (NO) levels in wild-type Arabidopsis (Arabidopsis thaliana) was accompanied by up-regulation of root FCR activity and the expression of the basic helix-loop-helix transcription factor (FIT) and the ferric reduction oxidase 2 (FRO2) genes. This was further stimulated by application of exogenous auxin (a-naphthaleneacetic acid) or NO donor (S-nitrosoglutathione [GSNO]), but suppressed by either polar auxin transport inhibition with 1-naphthylphthalamic acid or NO scavenging with 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, tungstate, or N v -nitro-L-arginine methyl ester hydrochloride. On the other hand, the root FCR activity, NO level, and gene expression of FIT and FRO2 were higher in auxin-overproducing mutant yucca under Fe deficiency, which were sharply restrained by 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide treatment. The opposite response was observed in a basipetal auxin transport impaired mutant aux1-7, which was slightly rescued by exogenous GSNO application. Furthermore, Fe deficiency or a-naphthaleneacetic acid application failed to induce Fe-deficiency responses in noa1 and nial nia2, two mutants with reduced NO synthesis, but root FCR activities in both mutants could be significantly elevated by GSNO. The inability to induce NO burst and FCR activity was further verified in a double mutant yucca noa1 with elevated auxin production and reduced NO accumulation. Therefore, we presented a novel signaling pathway where NO acts downstream of auxin to activate root FCR activity under Fe deficiency in Arabidopsis.

Differential effects of nitrogen forms on cell wall phosphorus remobilization in rice (Oryza sativa) are mediated by nitric oxide, pectin content and the expression of the phosphate transporter OsPT2

“…Increased NO production in various plant species has been widely observed in response to nutrient deficiency in general (Chen et al, 2010b) and P deficiency in particular . Interestingly, in this study, we found that NO is involved in the P deficiency response in rice.…”

“…; García-Mata and Lamattina, 2001), high temperature in Lucerne, Switzerland, low temperature in tomato (Solanum lycopersicum), wheat, and maize (Cueto et al, 1996); Al toxicity in rice bean (Vigna umbellata; Zhou et al, 2012); Fe deficiency in Arabidopsis (Chen et al, 2010b); and P deficiency in white lupin (Lupinus albus; Meng et al, 2012). NO improves the growth of white lupin under P deficiency through inducing cluster-root development and citrate exudation .…”

N-3-Oxo-Decanoyl-l-Homoserine-Lactone Activates Auxin-Induced Adventitious Root Formation via Hydrogen Peroxide- and Nitric Oxide-Dependent Cyclic GMP Signaling in Mung Bean

“…Together, these results suggest that 3-O-C10-HL-accelerated polar auxin transport likely contributes to the generation of H 2 O 2 or NO. Auxin has previously been shown to simulate H 2 O 2 or NO generation in cucumber, tomato, and Arabidopsis (Joo et al, 2001;Pagnussat et al, 2003;Chen et al, 2010), but auxin did not stimulate NO generation in a tobacco (Nicotiana tabacum) suspension (Tun et al, 2001), suggesting that this is not a universal mechanism and may be context dependent. Plant alkamide as a lipid signal that acts as an AHL homolog can induce the accumulation of NO and adventitious root development in Arabidopsis (Campos-Cuevas et al, 2008), indicating that plants may have evolved a common mechanism to respond to exogenous AHLs, endogenous NAEs, and alkamide stimulation (Méndez-Bravo et al, 2010;MorquechoContreras et al, 2010).…”

Similarities and Differences in the Acquisition of Fe and P by Dicot Plants

“…In addition to ethylene, other hormones and signaling substances, such as auxin and nitric oxide (NO), have been involved in the up-regulation of Fe and P acquisition genes [3,4,29,68,[75][76][77][78][79][80][81]. In both deficiencies, the activating effect of auxin, ethylene and NO depend on the Fe or P status of the plants [68,69,75,76], which suggests the existence of additional Fe-and P-related signals acting in conjunction with ethylene, auxin and NO [82].…”