Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato

Shahnejat-Bushehri, Sara; Allu, Annapurna Devi; Mehterov, Nikolay; Thirumalaikumar, Venkatesh P.; Alseekh, Saleh; Fernie, Alisdair R.; Mueller‐Roeber, Bernd; Balazadeh, Salma

doi:10.3389/fpls.2017.00214

Cited by 29 publications

(23 citation statements)

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“…Furthermore, Al can trigger signal transduction pathways upon which phytohormones act [37]. In tomato, the overexpression of the Arabidopsis NAC transcription factor JUNGBRUNNEN1 (AtJUB1) exerts conserved control over gibberellin and brassinosteroid metabolism and signaling genes controlling growth [71]. Importantly, NAC genes may be regulated by ABA-dependent or ABA-independent pathways because of the difference in their promoter elements [72].…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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In acid soils, the solubilized form of aluminum, Al+3, decreases root growth and affects the development of most crops. However, like other toxic elements, Al can have hormetic effects on plant metabolism. Rice (Oryza sativa) is one of the most tolerant species to Al toxicity, and when this element is supplied at low doses, growth stimulation has been observed, which could be due to combined mechanisms that are partly triggered by NAC transcription factors. This protein family can regulate vital processes in plants, including growth, development, and response to environmental stimuli, whether biotic or abiotic. Under our experimental conditions, 200 μM Al stimulated root growth and the formation of tillers; it also caused differential expression of a set of NAC genes. The promoter regions of the genes regulated by Al were analyzed and the cis-acting elements that are potentially involved in the responses to different stimuli, including environmental stress, were identified. Through the Genevestigator platform, data on the expression of NAC genes were obtained by experimental condition, tissue, and vegetative stage. This is the first study on NAC genes where in vivo and in silico data are complementarily analyzed, relating the hormetic effect of Al on plant growth and gene expression with a possible interaction in the response to phytohormones in rice. These findings could help to elucidate the possible convergence between the signaling pathways mediated by phytohormones and the role of the NAC transcription factors in the regulation of growth mediated by low Al doses.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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“…In addition, proline, a likely important osmoprotectant in plants (Ashrafa and Fooladb, ), accumulated in MusaNAC042 overexpressors compared to control plants, concomitant with an improved tolerance to drought and high salinity stress (Tak et al ., ). Of note, elevated levels of proline, in addition to the osmoprotectant trehalose, were also detected in tissues of Arabidopsis and tomato AtJUB1 overexpressors (Shahnejat‐Bushehri et al ., ; Wu et al ., ), suggesting that compatible solute osmolytes contribute to the enhanced drought tolerance in these plants in accordance with the important role of osmotic adjustment during drought conditions (Blum, ).…”

Section: Discussionmentioning

confidence: 99%

“…In this study, we investigated the function of the NAC transcription factor JUNGBRUNNEN1 (JUB1) for the response of tomato to drought stress. Previously, we showed that JUB1 (ANAC042) from Arabidopsis thaliana (hereafter, AtJUB1) functions as a central regulator of plant longevity and the interplay between growth and stress responses (Shahnejat-Bushehri et al, 2016;Wu et al, 2012). We reported that AtJUB1 exerts its role in controlling the response to stress in part through dampening cellular hydrogen peroxide (H 2 O 2 ) level.…”

Section: Introductionmentioning

confidence: 99%

“…In a transcription factor control cascade, DREB2A is an upstream regulator of Heat-shock factor A2 (HsfA2) and thereby several HEAT-SHOCK PROTEIN (HSP) genes and genes encoding H 2 O 2 scavenging enzymes (Schramm et al, 2008;Yoshida et al, 2008). Furthermore, AtJUB1 directly represses the expression of genes encoding key enzymes of gibberellic acid (GA) and brassinosteroid (BR) biosynthesis; this reduces the levels of both growth hormones, thereby leading to the stabilization of DELLA proteins (Shahnejat-Bushehri et al, 2016). Additionally, AtJUB1 directly binds to the promoters of DELLA (GAI and RGL1) genes and positively regulates their expression.…”

Section: Introductionmentioning

confidence: 99%

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NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato

Thirumalaikumar

Devkar

Mehterov

et al. 2017

Plant Biotechnology Journal

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237

116

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SummaryWater deficit (drought stress) massively restricts plant growth and the yield of crops; reducing the deleterious effects of drought is therefore of high agricultural relevance. Drought triggers diverse cellular processes including the inhibition of photosynthesis, the accumulation of cell‐damaging reactive oxygen species and gene expression reprogramming, besides others. Transcription factors (TF) are central regulators of transcriptional reprogramming and expression of many TF genes is affected by drought, including members of the NAC family. Here, we identify the NAC factor JUNGBRUNNEN1 (JUB1) as a regulator of drought tolerance in tomato (Solanum lycopersicum). Expression of tomato JUB1 (SlJUB1) is enhanced by various abiotic stresses, including drought. Inhibiting SlJUB1 by virus‐induced gene silencing drastically lowers drought tolerance concomitant with an increase in ion leakage, an elevation of hydrogen peroxide (H2O2) levels and a decrease in the expression of various drought‐responsive genes. In contrast, overexpression of AtJUB1 from Arabidopsis thaliana increases drought tolerance in tomato, alongside with a higher relative leaf water content during drought and reduced H2O2 levels. AtJUB1 was previously shown to stimulate expression of DREB2A, a TF involved in drought responses, and of the DELLA genes GAI and RGL1. We show here that SlJUB1 similarly controls the expression of the tomato orthologs SlDREB1, SlDREB2 and SlDELLA. Furthermore, AtJUB1 directly binds to the promoters of SlDREB1, SlDREB2 and SlDELLA in tomato. Our study highlights JUB1 as a transcriptional regulator of drought tolerance and suggests considerable conservation of the abiotic stress‐related gene regulatory networks controlled by this NAC factor between Arabidopsis and tomato.

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“…The NAC factor JUNGBRUNNEN1 (JUB1) negatively regulates senescence, while it positively affects tolerance to various abiotic stresses (Wu et al ., ; Ebrahimian‐Motlagh et al ., ). Metabolite profiling revealed elevated levels of proline and trehalose in JUB1 overexpressors (Wu et al ., ; Shahnejat‐Bushehri et al ., ). However, it is currently unknown whether genes affecting the metabolite levels are directly controlled by JUB1.…”

Section: Introductionmentioning

confidence: 97%

Transcription factor RD26 is a key regulator of metabolic reprogramming during dark‐induced senescence

et al. 2018

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SummaryLeaf senescence is a key process in plants that culminates in the degradation of cellular constituents and massive reprogramming of metabolism for the recovery of nutrients from aged leaves for their reuse in newly developing sinks.We used molecular-biological and metabolomics approaches to identify NAC transcription factor (TF) RD26 as an important regulator of metabolic reprogramming in Arabidopsis thaliana.RD26 directly activates CHLOROPLAST VESICULATION (CV), encoding a protein crucial for chloroplast protein degradation, concomitant with an enhanced protein loss in RD26 overexpressors during senescence, but a reduced decline of protein in rd26 knockout mutants. RD26 also directly activates LKR/SDH involved in lysine catabolism, and PES1 important for phytol degradation. Metabolic profiling revealed reduced c-aminobutyric acid (GABA) in RD26 overexpressors, accompanied by the induction of respective catabolic genes. Degradation of lysine, phytol and GABA is instrumental for maintaining mitochondrial respiration in carbon-limiting conditions during senescence.RD26 also supports the degradation of starch and the accumulation of mono-and disaccharides during senescence by directly enhancing the expression of AMY1, SFP1 and SWEET15 involved in carbohydrate metabolism and transport. Collectively, during senescence RD26 acts by controlling the expression of genes across the entire spectrum of the cellular degradation hierarchy.

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Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato

Cited by 29 publications

References 81 publications

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

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

NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato

Transcription factor RD26 is a key regulator of metabolic reprogramming during dark‐induced senescence

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