Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway

Abstract

To compete for nutrients in diverse soil microenvironments, plants proliferate lateral roots preferentially in nutrient-rich zones. For nitrate, root foraging involves local and systemic signaling; however, little is known about the genes that function in the systemic signaling pathway. By using nitrate enhancer DNA to screen a library of Arabidopsis transcription factors in the yeast one-hybrid system, the transcription factor gene TEOSINTE BRANCHED1/CYCLO-IDEA/PROLIFERATING CELL FACTOR1-20 (TCP20) was identified. TCP20, which belongs to an ancient, plant-specific gene family that regulates shoot, flower, and embryo development, was implicated in nitrate signaling by its ability to bind DNA in more than 100 nitrate-regulated genes. Analysis of insertion mutants of TCP20 showed that they had normal primary and lateral root growth on homogenous nitrate media but were impaired in preferential lateral root growth (root foraging) on heterogeneous media in split-root plates. Inhibition of preferential lateral root growth was still evident in the mutants even when ammonium was uniformly present in the media, indicating that the TCP20 response was to nitrate. Comparison of tcp20 mutants with those of nlp7 mutants, which are defective in local control of root growth but not in the root-foraging response, indicated that TCP20 function is independent of and distinct from NLP7 function. Further analysis showed that tcp20 mutants lack systemic control of root growth regardless of the local nitrate concentrations. These results indicate that TCP20 plays a key role in the systemic signaling pathway that directs nitrate foraging by Arabidopsis roots. TCP20 | nitrate | root foraging | systemic signaling | Arabidopsis

Cell Type-Specific Gene Expression Analyses by RNA Sequencing Reveal Local High Nitrate-Triggered Lateral Root Initiation in Shoot-Borne Roots of Maize by Modulating Auxin-Related Cell Cycle Regulation

“…Local nitrate remodels lateral root patterning by local signaling and in dependence of systemic regulation Forde, 2014;Guan et al, 2014). Impressive progress has been made in understanding the mechanisms regulating lateral root development in roots of Arabidopsis (Giehl and von Wirén, 2014) and crops (von Behrens et al, 2011;Smith and De Smet, 2012;Orman-Ligeza et al, 2013).…”

“…In resource-depleted environments, an important heterogeneously distributed soil factor is nutrient availability, which then directs lateral root growth preferentially into nutrient-rich patches (Zhang and Forde, 1998;Lima et al, 2010;Giehl et al, 2012). Such directed lateral root development depends on regulatory networks that integrate both local and systemic signals to coordinate them with the overall plant nutritional status Guan et al, 2014). As shown by the impact of the N status-dependent regulatory module CLAVATA3/ EMBRYO-SURROUNDING REGION-related peptides-CLAVATA1 leucine-rich repeat receptor-like kinase, economizing the costs for root development is pivotal for a resource-efficient strategy in nutrient acquisition (Araya et al, 2014).…”

Living to Die and Dying to Live: The Survival Strategy behind Leaf Senescence

“…In particular, the root system utilizes a sophisticated foraging strategy to find novel nutrient resources once those in the immediate vicinity become depleted. To support root foraging, it is sometimes essential to recycle leaves to sustain root growth (Guan et al, 2014;Higuchi et al, 2014). Under both agricultural and natural field conditions, plants grow in dense stands, where they must compete for resources.…”

TheArabidopsis thalianaTCP transcription factors: A broadening horizon beyond development

“…51 Very recently, yeast one-hybrid assays have identified a crucial role for TCP20 in the systemic signaling pathway that directs nitrate foraging by Arabidopsis roots. 81 Strikingly, some effects of TCP proteins on plant growth and development are mediated by their participation in the biosynthesis of bioactive metabolites, including brassinosteroids (BRs), jasmonic acid (JA) and flavonoids. 19,60,[66][67][68] As the natural polyhydroxy steroidal phytohormones, brassinosteroids (BRs) play crucial roles in multiple physiological processes ranging from seed germination to leaf senescence.…”