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

ABSTRACT: 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.

SUBMITTER: Mora-Macias J

PROVIDER: S-EPMC5410833 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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

Mora-Macías Javier J Ojeda-Rivera Jonathan Odilón JO Gutiérrez-Alanís Dolores D Yong-Villalobos Lenin L Oropeza-Aburto Araceli A Raya-González Javier J Jiménez-Domínguez Gabriel G Chávez-Calvillo Gabriela G Rellán-Álvarez Rubén R Herrera-Estrella Luis L

Proceedings of the National Academy of Sciences of the United States of America 20170411 17

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 <i>Arabidopsis</i>, 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 d ...[more]

PMID: 28400510

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Project description:To gain a genome-scale understanding of the role that developmental processes play in regulating stimulus response, we examined the effect of -Fe stress on gene expression along the longitudinal axis of the root. Since roots grow from stem cells located near the tip, the position of cells along the longitudinal axis can be used as a proxy for developmental time, with distance from the root tip correlating with increased differentiation. To estimate the role developmental stage plays in regulating salt response, roots were dissected into four longitudinal zones (LZ data set) after transfer to standard or -Fe media and transcriptionally profiled. Little is known about how developmental cues affect the way cells interpret their environment. Here we characterize the transcriptional response of different cell layers and developmental stages of the Arabidopsis root to high salinity and find that transcriptional responses are highly constrained by developmental parameters. These transcriptional changes lead to the differential regulation of specific biological functions in subsets of cell-layers, several of which correspond to observable physiological changes. We show that known stress pathways primarily control semi-ubiquitous responses and use mutants that disrupt epidermal patterning to reveal cell-layer specific and inter-cell-layer effects. By performing a similar analysis using iron-deprivation we identify common cell-type specific stress responses and environment-independent biological functions that define each cell type. Experiment Overall Design: Roots were grown under standard conditions for 5 days then transfered to standard media or iron deficient (-Fe) conditions (0.3mM Ferrozine in MS media containing no ferrous sulfate). 24 hours after transferring seedlings, roots were cut into 4 regions using a razor blade. The first cut was made ~150 Âµm from the root tip at the point where the shape of the root transitions from conical to cylindrical (Zone 1). The second cut was made ~200 Âµm above the first cut, at the point were the root becomes less optically dense, which marks the approximate end of the meristematic zone (Zone 2). The third cut was made ~200-300 Âµm above the second cut, just below the region where root hairs begin to emerge (Zone 3). The fourth cut was made ~1 mm above the third cut (Zone 4).

Dataset Information

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

Publications

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

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