Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation

Balzergue, Coline; Dartevelle, Thibault; Godon, Christian; Laugier, Edith; Meisrimler, Claudia-Nicole; Teulon, Jean‐Marie; Creff, Audrey; Bissler, Marie; Brouchoud, Corinne; Hagège, Agnès; Müller, Jens; Chiarenza, Serge; Javot, Hélène; Bécuwe-Linka, Noëlle; David, Pascale; Péret, Benjamin; Delannoy, Étienne; Thibaud, Marie-Christine; Armengaud, Jean; Abel, Steffen; Pellequer, Jean‐Luc; Nussaume, Laurent; Desnos, Thierry

doi:10.1038/ncomms15300

Cited by 279 publications

(360 citation statements)

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“…We used the pALMT1::GUS ( GUS , uidA gene encoding β‐glucuronidase) construct to investigate the role of Fe because this visual reporter sensitively allows to test the activity of STOP1 signaling in the root tip (Balzergue et al ., ). We first tested the influence of the Pi/Fe ratio on the expression of ALMT1 .…”

Section: Resultsmentioning

confidence: 97%

“…A large‐scale forward genetics screen for seedlings with a primary root less sensitive to –Pi inhibition identified several stop1 and almt1 mutants (in addition to lpr1 ) (Balzergue et al ., ). SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) is a C 2 H 2 zinc finger transcription factor necessary for the expression of ALUMINUM ACTIVATED MALATE TRANSPORTER 1 ( ALMT1 ), encoding a plasma membrane transporter exuding malate (Hoekenga et al ., ; Iuchi et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…In the root tip, Pi deprivation enhances the transcript level of ALMT1 but not of STOP1 , suggesting post‐translational regulation of STOP1 protein. Indeed, the –Pi condition stimulates the accumulation of STOP1 in the nucleus (Balzergue et al ., ). This nuclear accumulation of STOP1 therefore represents an important control step in this pathway for which a first, and unexpected, regulatory component has been identified recently.…”

Section: Introductionmentioning

confidence: 97%

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Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

et al. 2019

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Summary Low‐phosphate (Pi) conditions are known to repress primary root growth of Arabidopsis at low pH and in an Fe‐dependent manner. This growth arrest requires accumulation of the transcription factor STOP1 in the nucleus, where it activates the transcription of the malate transporter gene ALMT1; exuded malate is suspected to interact with extracellular Fe to inhibit root growth. In addition, ALS3 – an ABC‐like transporter identified for its role in tolerance to toxic Al – represses nuclear accumulation of STOP1 and the expression of ALMT1. Until now it was unclear whether Pi deficiency itself or Fe activates the accumulation of STOP1 in the nucleus. Here, by using different growth media to dissociate the effects of Fe from Pi deficiency itself, we demonstrate that Fe is sufficient to trigger the accumulation of STOP1 in the nucleus, which, in turn, activates the expression of ALMT1. We also show that a low pH is necessary to stimulate the Fe‐dependent accumulation of nuclear STOP1. Furthermore, pharmacological experiments indicate that Fe inhibits proteasomal degradation of STOP1. We also show that Al acts like Fe for nuclear accumulation of STOP1 and ALMT1 expression, and that the overaccumulation of STOP1 in the nucleus of the als3 mutant grown in low‐Pi conditions could be abolished by Fe deficiency. Altogether, our results indicate that, under low‐Pi conditions, Fe2/3+ and Al3+ act similarly to increase the stability of STOP1 and its accumulation in the nucleus where it activates the expression of ALMT1.

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

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Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

et al. 2019

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“…A previous study showed that the inhibition of primary root growth occurred within several hours under Pi deficiency (Balzergue et al, 2017). Root growth is caused by both cell elongation and cell division.…”

Section: Hdc1 Derepresses Primary Root Growth By Inhibiting Cell Elonmentioning

confidence: 98%

“…PDR2 encodes a P5-type ATPase, whereas LPR1/2 is a ferroxidase, which enables ROS generation and callose deposition in both the apoplast surrounding the stem cell niche (SCN) of the root apical meristem (RAM) and the root transition zone. Recently, it was also reported that mutants of other Al tolerance genes, stop1 and almt1, are both insensitive to Pi deficiency in terms of primary root growth inhibition (Balzergue et al, 2017;Mora-Mac ıas et al, 2017). The hsp10 allele is a loss-of-function allele of ALUMINUM SENSITIVE3 (ALS3), which encodes a half-size ABC transporter involved in Al resistance (Xu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Low phosphate represses histone deacetylase complex1 to regulate root system architecture remodeling in Arabidopsis

Wang

et al. 2019

New Phytologist

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The mechanisms involved in the regulation of gene expression in response to phosphate (Pi) deficiency have been extensively studied, but their chromatin-level regulation remains poorly understood.We examined the role of histone acetylation in response to Pi deficiency by using the histone deacetylase complex1 (hdc1) mutant. Genes involved in root system architecture (RSA) remodeling were analyzed by quantitative real-time polymerase chain reaction (qPCR) and chromatin immunoprecipitation qPCR.We demonstrate that histone H3 acetylation increased under Pi deficiency, and the hdc1 mutant was hypersensitive to Pi deficiency, with primary root growth inhibition and increases in root hair number. Concomitantly, Pi deficiency repressed HDC1 protein abundances. Under Pi deficiency, hdc1 accumulated higher concentrations of Fe 3+ in the root tips and had higher expression of genes involved in RSA remodeling, such as ALUMINUM-ACTIVATED MALATE TRANSPORTER1 (ALMT1), LOW PHOSPHATE ROOT1 (LPR1), and LPR2 compared with wild-type plants. Furthermore, Pi deficiency enriched the histone H3 acetylation of ALMT1 and LPR1. Finally, genetic evidence showed that LPR1/2 was epistatic to HDC1 in regulating RSA remodeling.Our results suggest a chromatin-level control of Pi starvation responses in which HDC1-mediated histone H3 deacetylation represses the transcriptional activation of genes involved in RSA remodeling in Arabidopsis.

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Approaches and determinants to sustainably improve crop production

Gojon

Nussaume

Luu

et al. 2022

Food and Energy Security

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Plant scientists and farmers are facing major challenges in providing food and nutritional security for a growing population, while preserving natural resources and biodiversity. Moreover, this should be done while adapting agriculture to climate change and by reducing its carbon footprint. To address these challenges, there is an urgent need to breed crops that are more resilient to suboptimal environments. Huge progress has recently been made in understanding the physiological, genetic and molecular bases of plant nutrition and environmental responses, paving the way towards a more sustainable agriculture. In this review, we present an overview of these progresses and strategies that could be developed to increase plant nutrient use efficiency and tolerance to abiotic stresses. As illustrated by many examples, they already led to promising achievements and crop improvements. Here, we focus on nitrogen and phosphate uptake and use efficiency and on adaptation to drought, salinity and heat stress. These examples first show the necessity of deepening our physiological and molecular understanding of plant environmental responses. In particular, more attention should be paid to investigate stress combinations and stress recovery and acclimation that have been largely neglected to date. It will be necessary to extend these approaches from model plants to crops, to unravel the relevant molecular targets of biotechnological or genetic strategies directly in these species. Similarly, sustained efforts should be done for further exploring the genetic resources available in these species, as well as in wild species adapted to unfavourable environments. Finally, technological developments will be required to breed crops that are more resilient and efficient. This especially relates to the development of multiscale phenotyping under field conditions and a wide range of environments, and use of modelling and big data management to handle the huge amount of information provided by the new molecular, genetic and phenotyping techniques.

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Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation

Cited by 279 publications

References 77 publications

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

Low phosphate represses histone deacetylase complex1 to regulate root system architecture remodeling in Arabidopsis

Approaches and determinants to sustainably improve crop production

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