Aluminum Enhances Growth and Sugar Concentration, Alters Macronutrient Status and Regulates the Expression of NAC Transcription Factors in Rice

Abstract

Aluminum (Al) is a beneficial element for some plant species, especially when used at low concentrations. Though some transcription factors are induced by exposure to this element, no data indicate that Al regulates the expression of NAC genes in rice. In this study we tested the effect of applying 200 μM Al on growth, chlorophyll, amino acids, sugars, macronutrient concentration and regulation of NAC transcription factors gene expression in 24-day-old plants of four rice (Oryza sativa ssp. indica) cultivars: Cotaxtla, Tres Ríos, Huimanguillo and Temporalero, grown hydroponically under greenhouse conditions. Twenty days after treatment, we observed that Al enhanced growth in the four cultivars studied. On average, plants grown in the presence of Al produced 140% more root dry biomass and were 30% taller than control plants. Cotaxtla and Temporalero showed double the root length, while Huimanguillo and Cotaxtla had three times more root fresh biomass and 2.5 times more root dry biomass. Huimanguillo plants showed 1.5 times more shoot height, while Cotaxtla had almost double the root dry biomass. With the exception of Tres Ríos, the rest of the cultivars had almost double the chlorophyll concentration when treated with Al, whereas amino acid and proline concentrations were not affected by Al. Sugar concentration was also increased in plants treated with Al, almost 11-fold in comparison to the control. Furthermore, we observed a synergic response of Al application on P and K concentration in roots, and on Mg concentration in shoots. Twenty-four hours after Al treatment, NAC transcription factors gene expression was measured in roots by quantitative RT-PCR. Of the 57 NAC transcription factors genes primer-pairs tested, we could distinguish that 44% (25 genes) showed different expression patterns among rice cultivars, with most of the genes induced in Cotaxtla and Temporalero plants. Of the 25 transcription factors up-regulated, those showing differential expression mostly belonged to the NAM subfamily (56%). We conclude that Al improves growth, increases sugar concentration, P and K concentrations in roots, and Mg concentration in shoots, and report, for the first time, that Al differentially regulates the expression of NAC transcription factors in rice.

Expression patterns and promoter analyses of aluminum-responsive NAC genes suggest a possible growth regulation of rice mediated by aluminum, hormones and NAC transcription factors

“…Nevertheless, crops are negatively affected by different types of stress, including aluminum (Al) toxicity. Al is an important constituent of soils; it is the third most abundant element in the Earth’s crust, after oxygen (O) and silicon (Si), making up 7% of the mass [1]. Under acid soil conditions (pH < 5.0), Al adopts a trivalent form, Al +3 , which is toxic to plants, especially when found in high concentrations [2].…”

“…When rice is exposed to toxic levels of Al, the ASR transcription factors act concertedly and complementarily, recognizing the cis -acting elements in the promoters of the STAR1 gene to potentiate the Al response expression of a set of target genes [15–17]. Another family of transcription factors that responds to Al is NAC [1,18], which are specific to plants [19–21]. The acronym, NAC, derives from three genes that codify the NAC domain: NAM (for no apical meristem ), ATAF1/2 (for Arabidopsis thaliana Activation Factor 1/2 ), and CUC2 (for cup-shaped cotyledon 2 ).…”

“…The acronym, NAC, derives from three genes that codify the NAC domain: NAM (for no apical meristem ), ATAF1/2 (for Arabidopsis thaliana Activation Factor 1/2 ), and CUC2 (for cup-shaped cotyledon 2 ). They have multiple cell functions, including growth and development regulation, as well as responses to environmental stimuli like heat, cold, salinity, drought, and Al [1,18,22–26]. …”

“…Subsequently, Al was reported to have increased the concentration of chlorophylls ( a and b ) and carotenoids [28]. Recently, it was observed that 200 μM Al in 4 cultivars (Cotaxtla, Tres Ríos, Huimanguillo, and Temporalero) stimulated growth, increased the concentrations of chlorophylls and total soluble sugars in the plantlet, and augmented P and K concentrations in the root [1]. Beneficial effects of Al have also been reported in other crops.…”

“…The first study suggesting a possible involvement of NAC genes in Al responses reported that the OsNAC5 ( Os11g08210 ) gene is responsive to this metal in roots of maize plants exposed to Al for 24 h [18]. Moreover, differential expression in a group of 25 NAC genes in the roots of four different rice cultivars in response to Al stimuli was also observed [1]. …”