Phosphate Starvation Induces a Determinate Developmental Program in the Roots of Arabidopsis thaliana

Sánchez-Calderón, Lenin; López‐Bucio, José; Chacón-López, Alejandra; Cruz‐Ramírez, Alfredo; Nieto-Jacobo, Marı́a Fernanda; Dubrovsky, Joseph G.; Herrera-Estrella, Luis

doi:10.1093/pcp/pci011

Cited by 323 publications

(259 citation statements)

References 32 publications

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“…Such remodeling of RSA results in an increased root surface area for Pi absorption. The remodeling process begins with a reduction of cell elongation followed by the progressive loss of meristematic cells (Sánchez-Calderón et al, 2005). At later stages, cell proliferation is arrested, and cell differentiation takes place at the former meristematic and elongation regions of the primary root.…”

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confidence: 99%

Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency

Kang

Tian

et al. 2014

Plant Physiology

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Plants cope with inorganic phosphate (Pi) deficiencies in their environment by adjusting their developmental programs and metabolic activities. For Arabidopsis (Arabidopsis thaliana), the developmental responses include the inhibition of primary root growth and the enhanced formation of lateral roots and root hairs. Pi deficiency also inhibits photosynthesis by suppressing the expression of photosynthetic genes. Early studies showed that photosynthetic gene expression was also suppressed in Pi-deficient roots, a nonphotosynthetic organ; however, the biological relevance of this phenomenon remains unknown. In this work, we characterized an Arabidopsis mutant, hypersensitive to Pi starvation7 (hps7), that is hypersensitive to Pi deficiency; the hypersensitivity includes an increased inhibition of root growth. HPS7 encodes a tyrosylprotein sulfotransferase. Accumulation of HPS7 proteins in root tips is enhanced by Pi deficiency. Comparative RNA sequencing analyses indicated that the expression of many photosynthetic genes is activated in roots of hps7. Under Pi deficiency, the expression of photosynthetic genes in hps7 is further increased, which leads to enhanced accumulation of chlorophyll, starch, and sucrose. Pi-deficient hps7 roots also produce a high level of reactive oxygen species. Previous research showed that the overexpression of GOLDEN-like (GLK) transcription factors in transgenic Arabidopsis activates photosynthesis in roots. The GLK overexpressing (GLK OX) lines also exhibit increased inhibition of root growth under Pi deficiency. The increased inhibition of root growth in hps7 and GLK OX lines by Pi deficiency was completely reversed by growing the plants in the dark. Based on these results, we propose that suppression of photosynthetic gene expression is required for sustained root growth under Pi deficiency.

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confidence: 99%

Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency

Kang

Tian

et al. 2014

Plant Physiology

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“…This mechanism includes the transcriptional activation of high-affinity Pi transporters and the excretion of RNases, acid phosphatases, and organic acids (3)(4)(5). (ii) Changes in the architecture of the root system that reflect alterations in cell length, root meristem activity, root hair elongation, and an increased number of lateral roots (6,7). These changes presumably increase the exploratory capacity of the root and the absorptive surface area.…”

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Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots

Cruz‐Ramírez¹,

Oropeza-Aburto²,

Razo-Hernández³

et al. 2006

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

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Low phosphate (Pi) availability is one of the major constraints for plant productivity in natural and agricultural ecosystems. Plants have evolved a myriad of developmental and biochemical mechanisms to increase internal Pi uptake and utilization efficiency. One important biochemical pathway leading to an increase in internal Pi availability is the hydrolysis of phospholipids. Hydrolyzed phospholipids are replaced by nonphosphorus lipids such as galactolipids and sulfolipids, which help to maintain the functionality and structure of membrane systems. Here we report that a member of the Arabidopsis phospholipase D gene family (PLDZ2) is gradually induced upon Pi starvation in both shoots and roots. From lipid content analysis we show that an Arabidopsis pldz2 mutant is defective in the hydrolysis of phospholipids and has a reduced capacity to accumulate galactolipids under limiting Pi conditions. Morphological analysis of the pldz2 root system shows a premature change in root architecture in response to Pi starvation. These results show that PLDZ2 is involved in the eukaryotic galactolipid biosynthesis pathway, specifically in hydrolyzing phosphatidylcholine and phosphatidylethanolamine to produce diacylglycerol for digalactosyldiacylglycerol synthesis and free Pi to sustain other Pi-requiring processes.phosphate starvation ͉ phospholipids ͉ root architecture ͉ sulfolipids P hosphate (Pi) influences virtually all developmental and biochemical processes in plants. Pi is not only a constituent of key cell molecules such as ATP, nucleic acids, and phospholipids, but it is also a pivotal metabolic regulator of many processes including energy transfer, protein activation, and carbon and nitrogen metabolism. However, Pi availability can be one of the major constraints for plant growth in both natural and agricultural ecosystems because of its low mobility and high absorption capacity in the soil. As a response to this limitation, plants have evolved a range of developmental, biochemical, and symbiotic adaptive strategies to cope with low Pi availability (1, 2). In Arabidopsis, a general, 3-fold strategy to cope with low Pi availability has been described. (i) The release and uptake of Pi from external sources that are not readily available for plant uptake. This mechanism includes the transcriptional activation of high-affinity Pi transporters and the excretion of RNases, acid phosphatases, and organic acids (3-5). (ii) Changes in the architecture of the root system that reflect alterations in cell length, root meristem activity, root hair elongation, and an increased number of lateral roots (6, 7). These changes presumably increase the exploratory capacity of the root and the absorptive surface area. (iii) Optimization of Pi utilization due to a wide range of metabolic alterations, and the mobilization of Pi from internal reserves by the hydrolysis of nucleic acids, proteins, and the recycling of Pi from membrane phospholipids.During Pi deprivation, the total content of diverse phospholipids such as phosphatidylcholin...

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“…Like transceptors 32,33 , ALA10 is subject to phosphorylation in planta at serine and threonine residues 20,21 , which suggests that it is subject to tight regulation. One of the first signs of phosphate starvation in A. thaliana is that the root enters a determinate developmental programme in which primary root growth is arrested and cell differentiation is promoted, thereby stimulating lateral root growth and increasing the root surface area 34 . Notably, in response to phosphate starvation, the roots of the ala10 mutant were longer than those of the wild type (Fig.…”

Section: Discussionmentioning

confidence: 99%

A phospholipid uptake system in the model plant Arabidopsis thaliana

et al. 2015

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Plants use solar energy to produce lipids directly from inorganic elements and are not thought to require molecular systems for lipid uptake from the environment. Here we show that Arabidopsis thaliana Aminophospholipid ATPase10 (ALA10) is a P4-type ATPase flippase that internalizes exogenous phospholipids across the plasma membrane, after which they are rapidly metabolized. ALA10 expression and phospholipid uptake are high in the epidermal cells of the root tip and in guard cells, the latter of which regulate the size of stomatal apertures to modulate gas exchange. ALA10-knockout mutants exhibit reduced phospholipid uptake at the root tips and guard cells and are affected in growth and transpiration. The presence of a phospholipid uptake system in plants is surprising. Our results suggest that one possible physiological role of this system is to internalize lysophosphatidylcholine, a signalling lipid involved in root development and stomatal control.

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Phosphate Starvation Induces a Determinate Developmental Program in the Roots of Arabidopsis thaliana

Cited by 323 publications

References 32 publications

Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency

Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency

Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots

A phospholipid uptake system in the model plant Arabidopsis thaliana

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