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 and apply this knowledge to generate new plant varieties with improved nutrient uptake and use efficiency.
Phosphorus (P) is a nutrient that limits crop yield in more than 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. These strategies include alterations in root system architecture and carbon metabolism, as well as excretion of enzymes and compounds with low molecular weight. Furthermore, the expression of numerous genes is enhanced, including 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. In addition, root meristematic activity is altered, resulting in a shallow root system with a high capacity for exploration of the upper layer of the soil, where 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, leading to the formation of roots specialized in P extraction from the soil.
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. These 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 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 roots 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 are 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 (i.e., a short primary root with an abundance of lateral roots and long root hairs). The former class of mutants appears to be affected either in the mechanisms of sensing the internal reserves of P or in 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.
Poor soil fertility and aggressive weeds pose major constraints to meeting the increasing demand for global food production. Starting with the green revolution in the 1960s, higher yields have been accompanied by a steady increase in the use of fertilizers and herbicides. Low Pi availability in the soil is mainly due to its high reactivity with soil components and rapid conversion by soil bacteria into organic forms that are not readily available for plant uptake. As a result of both of these factors, as little as 20 to 30 percent of the Pi that is applied as fertilizer is actually used by cultivated plants. The inefficient utilization of Pi present in fertilizer is further aggravated by the competition of weeds with crops for soil resources.
Because Pi cannot be substituted in plant nutrition, relatively little attention has been given to the use of other chemical forms of phosphorus to formulate effective and potentially less environmentally hazardous fertilizers. One proposal, after World War II, was the use of phosphite, a reduced form of phosphorus, as a promising alternative fertilizer, owing to its distinct chemical and biochemical properties compared with orthophosphate, including higher solubility, lower reactivity with soil components, and the inability of most microorganisms to use it as a phosphorus source. But plants cannot metabolize phosphite, limiting its use as a fertilizer. However, we developed a novel fertilization and weed control system by engineering plants to metabolize phosphite. This was achieved by expressing a phosphite oxidoreductase that converts phosphite into Pi in transgenic plants. When grown in soil that contains native microflora and is fertilized with phosphite, engineered plants expressing the phosphite oxidoreductase achieve maximum productivity with 30 to 50 percent less P than that required to reach the same productivity using Pi as fertilizer. Because nonengineered plants are unable to use phosphite as a P source, when fertilized with phosphite, the engineered plants easily outcompete weeds, reducing or eliminating the need for herbicides to achieve maximum yield.
In contrast to Pi, which when released from contaminated rivers into the ocean promotes toxic algal blooms that kill aquatic organisms, phosphite should not cause these severe ecological problems because it cannot be used as a nutrient by algae. Thus, these metabolically engineered plants allow the design of a dual fertilization and weed control system with both potentially important economical and ecological benefits.
As of September 26, 2012