Iron-Dependent Callose Deposition Adjusts Root Meristem Maintenance to Phosphate Availability

Müller, Jens; Toev, Theresa; Heisters, Marcus; Teller, Janine; Moore, Katie L.; Hause, Gerd; Dinesh, Dhurvas Chandrasekaran; Bürstenbinder, Katharina; Abel, Steffen

doi:10.1016/j.devcel.2015.02.007

Cited by 289 publications

(464 citation statements)

References 60 publications

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“…Accumulation of Fe in the apoplast of cells in the RAM is required to activate the primary root response to low Pi availability (20). As carboxylateiron complexes have been reported to participate in iron transport and acquisition in plants ( [28][29][30] and malate efflux is affected in stop1 and almt1 mutants (21,22), we explored whether malate exudation plays a role in the Fe accumulation mechanism that is required to trigger primary root growth inhibition in response to low Pi availability.…”

Section: Almt1 Is Expressed In the Ram Of Arabidopsis Under Pi-deficimentioning

confidence: 99%

“…Whereas the precise function of PDR2 has not been determined, LPR1 is essential for primary root inhibition under lowPi conditions and it has been shown to have ferroxidase activity (16,19,20). An LPR1-dependent accumulation of Fe +3 in the apoplast of cells in the elongation and meristematic regions of the primary root, that triggers the production of reactive oxygen species (ROS), is essential for meristem exhaustion in low-Pi media (20). ROS generation correlates with callose deposition in the RAM, which was proposed to activate meristem exhaustion by blocking the cell-to-cell movement of SHORT-ROOT (SHR), a transcription factor that is essential for stem cell maintenance in the RAM (20).…”

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confidence: 99%

“…PDR2 and LPR1 have been proposed to orchestrate RAM exhaustion in a genetically interacting route under low-Pi conditions (19). Whereas the precise function of PDR2 has not been determined, LPR1 is essential for primary root inhibition under lowPi conditions and it has been shown to have ferroxidase activity (16,19,20). An LPR1-dependent accumulation of Fe +3 in the apoplast of cells in the elongation and meristematic regions of the primary root, that triggers the production of reactive oxygen species (ROS), is essential for meristem exhaustion in low-Pi media (20).…”

mentioning

confidence: 99%

“…An LPR1-dependent accumulation of Fe +3 in the apoplast of cells in the elongation and meristematic regions of the primary root, that triggers the production of reactive oxygen species (ROS), is essential for meristem exhaustion in low-Pi media (20). ROS generation correlates with callose deposition in the RAM, which was proposed to activate meristem exhaustion by blocking the cell-to-cell movement of SHORT-ROOT (SHR), a transcription factor that is essential for stem cell maintenance in the RAM (20). However, the mechanism that regulates iron accumulation and relocation in the RAM remains largely unknown.…”

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confidence: 99%

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Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Mora-Macías

Ojeda-Rivera

Gutiérrez-Alanís

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

244

153

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Low phosphate (Pi) availability constrains plant development and seed production in both natural and agricultural ecosystems. When Pi is scarce, modifications of root system architecture (RSA) enhance the soil exploration ability of the plant and lead to an increase in Pi uptake. In Arabidopsis, an iron-dependent mechanism reprograms primary root growth in response to low Pi availability. This program is activated upon contact of the root tip with low-Pi media and induces premature cell differentiation and the arrest of mitotic activity in the root apical meristem, resulting in a short-root phenotype. However, the mechanisms that regulate the primary root response to Pi-limiting conditions remain largely unknown. Here we report on the isolation and characterization of two low-Pi insensitive mutants (lpi5 and lpi6), which have a long-root phenotype when grown in low-Pi media. Cellular, genomic, and transcriptomic analysis of low-Pi insensitive mutants revealed that the genes previously shown to underlie Arabidopsis Al tolerance via root malate exudation, known as SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) and ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (ALMT1), represent a critical checkpoint in the root developmental response to Pi starvation in Arabidopsis thaliana. Our results also show that exogenous malate can rescue the long-root phenotype of lpi5 and lpi6. Malate exudation is required for the accumulation of Fe in the apoplast of meristematic cells, triggering the differentiation of meristematic cells in response to Pi deprivation.

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Section: Almt1 Is Expressed In the Ram Of Arabidopsis Under Pi-deficimentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Mora-Macías

Ojeda-Rivera

Gutiérrez-Alanís

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

244

153

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“…For colocalization assays, images were obtained in the sequential mode. Root cells of transgenic Arabidopsis seedlings were plasmolyzed by treatment with 150 mM NaCl as described by Müller et al (2015). For PI or FM4-64 staining, cells were incubated for 1 to 5 min in 10 mM PI or 50 mM Synapto-Red C2, respectively.…”

Section: Confocal Laser Scanning Microscopymentioning

confidence: 99%

The IQD Family of Calmodulin-Binding Proteins Links Calcium Signaling to Microtubules, Membrane Subdomains, and the Nucleus

et al. 2017

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ORCID IDs: 0000-0002-3493-4800 (K.B.); 0000-0002-7146-043X (B.M.).Calcium (Ca 2+ ) signaling and dynamic reorganization of the cytoskeleton are essential processes for the coordination and control of plant cell shape and cell growth. Calmodulin (CaM) and closely related calmodulin-like (CML) polypeptides are principal sensors of Ca 2+ signals. CaM/CMLs decode and relay information encrypted by the second messenger via differential interactions with a wide spectrum of targets to modulate their diverse biochemical activities. The plant-specific IQ67 DOMAIN (IQD) family emerged as possibly the largest class of CaM-interacting proteins with undefined molecular functions and biological roles. Here, we show that the 33 members of the IQD family in Arabidopsis (Arabidopsis thaliana) differentially localize, using green fluorescent protein (GFP)-tagged proteins, to multiple and distinct subcellular sites, including microtubule (MT) arrays, plasma membrane subdomains, and nuclear compartments. Intriguingly, the various IQD-specific localization patterns coincide with the subcellular patterns of IQD-dependent recruitment of CaM, suggesting that the diverse IQD members sequester Ca 2+ -CaM signaling modules to specific subcellular sites for precise regulation of Ca 2+ -dependent processes. Because MT localization is a hallmark of most IQD family members, we quantitatively analyzed GFP-labeled MT arrays in Nicotiana benthamiana cells transiently expressing GFP-IQD fusions and observed IQD-specific MT patterns, which point to a role of IQDs in MT organization and dynamics. Indeed, stable overexpression of select IQD proteins in Arabidopsis altered cellular MT orientation, cell shape, and organ morphology. Because IQDs share biochemical properties with scaffold proteins, we propose that IQD families provide an assortment of platform proteins for integrating CaM-dependent Ca 2+ signaling at multiple cellular sites to regulate cell function, shape, and growth.

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Sorghum root epigenetic landscape during limiting phosphorus conditions

Gladman

Hufnagel²,

Regulski

et al. 2022

Plant Direct

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Efficient acquisition and use of available phosphorus from the soil is crucial for plant growth, development, and yield. With an ever‐increasing acreage of croplands with suboptimal available soil phosphorus, genetic improvement of sorghum germplasm for enhanced phosphorus acquisition from soil is crucial to increasing agricultural output and reducing inputs, while confronted with a growing world population and uncertain climate. Sorghum bicolor is a globally important commodity for food, fodder, and forage. Known for robust tolerance to heat, drought, and other abiotic stresses, its capacity for optimal phosphorus use efficiency (PUE) is still being investigated for optimized root system architectures (RSA). Whilst a few RSA‐influencing genes have been identified in sorghum and other grasses, the epigenetic impact on expression and tissue‐specific activation of candidate PUE genes remains elusive. Here, we present transcriptomic, epigenetic, and regulatory network profiling of RSA modulation in the BTx623 sorghum background in response to limiting phosphorus (LP) conditions. We show that during LP, sorghum RSA is remodeled to increase root length and surface area, likely enhancing its ability to acquire P. Global DNA 5‐methylcytosine and H3K4 and H3K27 trimethylation levels decrease in response to LP, while H3K4me3 peaks and DNA hypomethylated regions contain recognition motifs of numerous developmental and nutrient responsive transcription factors that display disparate expression patterns between different root tissues (primary root apex, elongation zone, and lateral root apex).

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Iron-Dependent Callose Deposition Adjusts Root Meristem Maintenance to Phosphate Availability

Cited by 289 publications

References 60 publications

Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

The IQD Family of Calmodulin-Binding Proteins Links Calcium Signaling to Microtubules, Membrane Subdomains, and the Nucleus

Sorghum root epigenetic landscape during limiting phosphorus conditions

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