Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci U S A, 107, 4477-4482

Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 02/2010; 107(9):4477-82. DOI: 10.1073/pnas.0909571107
Source: PubMed


One of the most striking examples of plant developmental plasticity to changing environmental conditions is the modulation of root system architecture (RSA) in response to nitrate supply. Despite the fundamental and applied significance of understanding this process, the molecular mechanisms behind nitrate-regulated changes in developmental programs are still largely unknown. Small RNAs (sRNAs) have emerged as master regulators of gene expression in plants and other organisms. To evaluate the role of sRNAs in the nitrate response, we sequenced sRNAs from control and nitrate-treated Arabidopsis seedlings using the 454 sequencing technology. miR393 was induced by nitrate in these experiments. miR393 targets transcripts that code for a basic helix-loop-helix (bHLH) transcription factor and for the auxin receptors TIR1, AFB1, AFB2, and AFB3. However, only AFB3 was regulated by nitrate in roots under our experimental conditions. Analysis of the expression of this miR393/AFB3 module, revealed an incoherent feed-forward mechanism that is induced by nitrate and repressed by N metabolites generated by nitrate reduction and assimilation. To understand the functional role of this N-regulatory module for plant development, we analyzed the RSA response to nitrate in AFB3 insertional mutant plants and in miR393 overexpressors. RSA analysis in these plants revealed that both primary and lateral root growth responses to nitrate were altered. Interestingly, regulation of RSA by nitrate was specifically mediated by AFB3, indicating that miR393/AFB3 is a unique N-responsive module that controls root system architecture in response to external and internal N availability in Arabidopsis.

Download full-text


Available from: Geraint Parry
  • Source
    • "The plates were incubated under the same growth conditions and root length was measured after 5 to 6 d. Hydroponic growth of plants on ammonium succinate medium was carried out essentially as described byVidal et al. (2010)with some modifications. Seeds were sown on a 250 mm stainless steel mesh cut to fit snugly in a GA-7 tissue culture vessel (Magenta). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Nitrogen is an essential soil nutrient for plants, and lack of nitrogen commonly limits plant growth. Soil nitrogen is typically available to plants in two inorganic forms: nitrate and ammonium. To better understand how nitrate and ammonium differentially affect plant metabolism and development, we performed transcriptional profiling of the shoots of ammonium-supplied and nitrate-supplied Arabidopsis thaliana plants. Seven genes encoding class III glutaredoxins were found to be strongly and specifically induced by nitrate. RNA silencing of four of these glutaredoxin genes (AtGRXS3/4/5/8) resulted in plants with increased primary root length (~25% longer than wild-type) and decreased sensitivity to nitrate-mediated inhibition of primary root growth. Increased primary root growth is also a well-characterized phenotype of many cytokinin-deficient plant lines. We determined that nitrate induction of glutaredoxin gene expression was dependent upon cytokinin signaling and that cytokinins could activate glutaredoxin gene expression independent of plant nitrate status. In addition, crosses between "long-root" cytokinin-deficient plants and "long-root" glutaredoxin-silenced plants generated hybrids that displayed no further increase in primary root length (i.e. epistasis). Collectively, these findings suggest that AtGRXS3/4/5/8 operate downstream of cytokinins in a signal transduction pathway that negatively regulates plant primary root growth in response to nitrate. This pathway could allow Arabidopsis to actively discriminate between different nitrogen sources in the soil, with the preferred nitrogen source, nitrate, acting to suppress primary root growth (vertical dimension) in concert with its well-characterized stimulatory effect on lateral root growth (horizontal dimension).
    Preview · Article · Dec 2015 · Plant physiology
  • Source
    • "Functional analyses have shown that miRNAs play critical roles in many developmental processes, including responses to abiotic and biotic stressors of plants. For example, miR156 controls leaf and flower development in Arabidopsis and rice (Wang et al. 2009, Wang et al. 2008, Xie et al. 2012), miR398 and miR408 are up-regulated in response to water deficiency in Medicago truncatula (Trindade et al. 2010), miR168 responds to abscisic acid stress (Li et al. 2012a), miR167 and miR393 regulate root development and help in adaptation to nitrogen deprivation (Gifford et al. 2008, Vidal et al. 2010), and miR395 controls the activity of the ATP sulfurylase gene (APS) and the high-affinity sulfate transporter gene (SULTR2;1) in response to sulfate starvation in Arabidopsis (Allen et al. 2005, Buhtz et al. 2010, Kawashima et al. 2009, Liang et al. 2010). Further, miR398, miR397, miR408, and miR857 have been shown to respond to copper deprivation (Abdel-Ghany and Pilon 2008, Naya et al. 2014, Sunkar et al. 2006, Yamasaki et al. 2007), and miR159, miR169, miR172, miR173, and miR394 have shown differential expression under iron starvation in Arabidopsis (Kong and Yang 2010). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Phosphorus (P) is an essential element involved in numerous biochemical reactions. In plants, stress responses, such as the expression of microRNAs (miRNAs), are induced to help them adapt to low phosphate (Pi) concentrations. In this study, deep sequencing was performed using the roots and leaves of maize seedlings grown under low Pi concentrations to identify miRNAs that are differentially expressed during the early stages of Pi deficiency. Eight small RNA libraries were constructed, and 159 known miRNAs representing 32 miRNA families and 10 novel miRNAs. Members of the miR396 family were extremely abundant. Further, 28 Pi-responsive miRNAs were identified (27 known and 1 novel) of which 8 and 7 were significantly expressed exclusively in leaf and root tissues, respectively. The analysis of Pi-responsive miRNAs target genes suggested that most target genes functioning as transcription factors were involved in root and leaf development. The expression profiles of selected Pi-responsive miRNAs and target genes were confirmed by qRT-PCR. Moreover, we discuss the significance of the differences in expression patterns of these miRNAs during the early and later stages of Pi starvation. The present study provides useful information concerning the role of miRNAs in response to Pi starvation and will further our understanding of the mechanisms governing Pi homeostasis in maize.
    Full-text · Article · Nov 2015 · Physiologia Plantarum
  • Source
    • "Since natural environments and agricultural fields have limited amounts of N, the production of high-yielding crops relies on the application of large quantities of nitrogenous fertilizers, which come at considerable economic (Good et al., 2004) and environmental costs (Hirel et al., 2011). The relevance of N for plants is clearly exemplified by its effects on leaf growth (von Wirén et al., 2000), senescence (Vanacker et al., 2006), root system architecture (Zhang et al., 2007; Vidal et al., 2010) and flowering time (Castro Marín et al., 2010). Besides growth and developmental effects, it is also clear that N nutrition can impact the plant's ability to cope with environmental challenges such as plant pathogen attacks (Snoeijers et al., 2000; Walters and Bingham, 2007; Dordas, 2008; Fagard et al., 2014). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Nitrogen (N) is one of the main limiting nutrients for plant growth and crop yield. It is well documented that changes in nitrate availability, the main N source found in agricultural soils, influences a myriad of developmental programs and processes including the plant defense response. Indeed, many agronomical reports indicate that the plant N nutritional status influences their ability to respond effectively when challenged by different pathogens. However, the molecular mechanisms involved in N-modulation of plant susceptibility to pathogens are poorly characterized. In this work, we show that Solanum lycopersicum defense response to the necrotrophic fungus Botrytis cinerea is affected by plant N availability, with higher susceptibility in nitrate-limiting conditions. Global gene expression responses of tomato against B. cinerea under contrasting nitrate conditions reveals that plant primary metabolism is affected by the fungal infection regardless of N regimes. This result suggests that differential susceptibility to pathogen attack under contrasting N conditions is not only explained by a metabolic alteration. We used a systems biology approach to identify the transcriptional regulatory network implicated in plant response to the fungus infection under contrasting nitrate conditions. Interestingly, hub genes in this network are known key transcription factors involved in ethylene and jasmonic acid signaling. This result positions these hormones as key integrators of nitrate and defense against B. cinerea in tomato plants. Our results provide insights into potential crosstalk mechanisms between necrotrophic defense response and N status in plants.
    Full-text · Article · Nov 2015 · Frontiers in Plant Science
Show more