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Sensory and Signaling Pathways Regulating Root Architecture during Phosphate Starvation
Summary: Research in Luis Herrera-Estrella's laboratory aims to understand how plants modify the architecture of their roots to improve their ability to obtain nutrients from the soil.
Phosphorus (P) is a nutrient that limits crop yield in over 30 percent of the world's arable land. To increase plant productivity in soils with low P availability, several million tons of P fertilizer are applied every year to agricultural soils. However, by some estimates, world resources of inexpensive P may be depleted by 2050. Therefore, improving a plant's ability to acquire and efficiently use P is critical to developing more sustainable agriculture. Plants have evolved a diverse array of adaptive strategies to obtain adequate P under conditions of low P availability. The strategies include alterations in root system architecture and carbon metabolism, as well as excretion of enzymes and low–molecular weight compounds. Furthermore, the expression of numerous genes is enhanced—genes involved in increasing a plant's capacity for soil exploration, its ability to extract and take up P from the soil, and its efficiency in the use of a scarce nutrient essential for plant growth and development. We are using Arabidopsis and maize to study the processes that are adaptive to low P availability. In Arabidopsis, we found that root system architecture is altered such that as the density of lateral roots increases, root hairs become longer; root meristematic activity is altered resulting in a shallow root with a high capacity for exploration of the upper layer of the soil, in which P-rich soil patches are more frequently found. We also determined that the roots of Arabidopsis plants subjected to low P enter a developmental program characterized by early differentiation of cells that exit the root meristem. The earliest event in this root growth program is that root stem cells divide; they later differentiate and actively transcribe genes involved in P uptake and scavenging, forming roots specialized in P extraction from the soil. We found that loss of stem cell activity was attributable to the negative regulation of plethora 1 and 2, two transcription factors involved in root meristem maintenance.
Lateral roots are formed from differentiated cells that are present in the pericycle, a cell layer surrounding the root vascular tissue. These cells must de-differentiate to initiate cell division and re-differentiate into the different cell types that form a lateral root. Auxin plays a central role in the de novo formation of lateral roots. Given that plants grown under low P conditions have an increased capacity to form lateral roots, we are interested in determining whether this capacity is mediated by a rise in the synthesis and transport of auxins or in auxin sensitivity of pericycle cells in these plants. Using several auxin-inducible gene markers and auxin transport inhibitors, we determined that augmented auxin sensitivity of the pericycle cells is the primary reason for the observed increase in lateral root formation in plants grown under low P conditions. Further work showed that the alteration in auxin sensitivity is attributable to the transcriptional regulation of genes encoding F-box proteins; the proteins are involved in ubiquitin-mediated degradation of transcription factors that repress the expression of auxin-responsive genes. We are currently investigating whether changes in hormone sensitivity are responsible for changes in the postembryonic root development program in response to the availability of other nutrients.
Given that resources are re-allocated to support an enhanced root growth under P deprivation, we are currently investigating how carbon flux from photosynthetic tissues is redirected to the root system to promote lateral root formation, which enhances the capacity of the plant to explore new soil horizons in the search for nutrients. We found that sucrose transport in the root of plants growing under optimal P conditions is directed to support the growth of the primary root; however, when these plants are transferred to conditions of low P availability, sucrose transport and unloading is directed to support the formation of lateral roots. To identify genes involved in the P response, we isolated chemical and T-DNA insertion mutants affected in the alteration of root system architecture in response to low P conditions. We identified two main classes of mutants, one in which primary root growth fails to be inhibited in low P conditions and the other a constitutive low P root phenotype (that is, short primary root with an abundance of lateral roots and long root hairs). The former class of mutants appear to be affected either in the mechanisms of sensing the internal reserves of P or enzymes involved in unloading sucrose from the phloem to the sites at which lateral roots are formed. We are currently investigating whether sensing the external concentration of P is affected in mutants that show a constitutive low P phenotype. The synthesis of phosphatidylcholine (PtdCho) is affected in one of the mutants with a low P constitutive phenotype (xpl1). Biochemical and cellular analyses of xpl1 suggest that molecules produced downstream of the PtdCho biosynthesis pathway, particularly phosphatidic acid, play key roles in root development and act as signals for cell integrity.
An important aspect of the biochemical responses of photosynthetic organisms to low Pi conditions is the replacement of phospholipids by non-phosphorous lipids, such as galactolipids, which allows the release of Pi from phospholipids to sustain other Pi-requiring cell activities. A global gene expression analysis of the Arabidopsis response to Pi deprivation showed that a member of the phospholipase D gene family is strongly upregulated by low Pi conditions. We identified insertion mutants in the PLDZ2 gene and subjected the mutants to lipid profile analysis. This analysis showed that PLDZ2 plays a major role in the hydrolysis of phospholipids to free Pi and to generate diacylglycerol, the direct substrate for the synthesis of galactolipids. To investigate whether the same classes of genes are activated during the low P response in maize, a crop of great economic and social importance in Mexico, we produced several differential and complete cDNA libraries of maize plants subjected to different times of P deprivation. To date, we have sequenced over 35,000 cDNA clones and have determined that many of the genes activated in Arabidopsis are also up regulated in maize.
Last updated October 2008
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