Global gene expression was analyzed in Arabidopsis (Arabidopsis thaliana) by microarrays comprising 21,500 genes. Leaf segments derived from phosphorus (P)-starved and P-replenished plants were incubated with or without sucrose (Suc) to obtain tissues with contrasting combinations of P and carbohydrate levels. Transcript profiling revealed the influence of the two factors individually and the interactions between P-and sugar-dependent gene regulation. A large number of gene transcripts changed more than 2-fold: In response to P starvation, 171 genes were induced and 16 repressed, whereas Suc incubation resulted in 337 induced and 307 repressed genes. A number of new candidate genes involved in P acquisition were discovered. In addition, several putative transcription factors and signaling proteins of P sensing were disclosed. Several genes previously identified to be sugar responsive were also regulated by P starvation and known P-responsive genes were sugar inducible. Nearly 150 genes were synergistically or antagonistically regulated by the two factors. These genes exhibit more prominent or contrasting regulation in response to Suc and P in combination than expected from the effect of the two factors individually. The genes exhibiting interactions form three main clusters with different response patterns and functionality of genes. One cluster (cluster 1) most likely represents a regulatory program to support increased growth and development when both P and carbohydrates are ample. Another cluster (cluster 3) represents genes induced to alleviate P starvation and these are further induced by carbohydrate accumulation. Thus, interactions between P and Suc reveal two different signaling programs and novel interactions in gene regulation in response to environmental factors. cis-Regulatory elements were analyzed for each factor and for interaction clusters. PHR1 binding sites were more frequent in promoters of P-regulated genes as compared to the entire Arabidopsis genome, and E2F and PHR1 binding sites were more frequent in interaction clusters 1 and 3, respectively.
Plants have evolved a number of adaptive strategies to cope with fluctuations in phosphorus (P) supply. The current knowledge of the transcriptional regulation of the P-starvation response in plants is limited. However, one MYB-related transcription factor, PHR1, is known to be involved in the P-starvation response. In this paper, we characterize a T-tagged phr1 knockout mutant and a series of transgenic plant lines which over-express PHR1 in wild type (WT) and phr1 mutant background. The knockout mutant has an altered phosphate (Pi) allocation between root and shoot; accumulates less anthocyanins, sugars and starch than P-starved WT; has a lower AGPase activity; and is impaired in induction of a subset of Pi starvation-induced genes. Expression of PHR1 in the phr1 mutant rescues the responsiveness to P-starvation and leads to WT levels of sugars and starch during Pi starvation conditions, confirming the involvement of PHR1 in adjusting carbon metabolism. Over-expression of PHR1 further resulted in a dramatic increase in the microRNA miR399d, and this resulted in changes in the transcript level for the target gene PHO2. Furthermore, over-expression of PHR1 in both WT and phr1 mutant results in strongly increased content of Pi irrespective of P regime. This shows that targeting a key regulatory element in the Pi starvation regulatory network represents a useful approach for molecular breeding of plants towards more efficient Pi uptake and assimilation.
Inorganic phosphate (Pi) is an essential nutrient for plants, and the low bioavailability of Pi in soils is often a limitation to growth and development. Consequently, plants have evolved a range of regulatory mechanisms to adapt to phosphorus-starvation in order to optimise uptake and assimilation of Pi. Recently, significant progress has been made in elucidating these mechanisms. The coordinated expression of a large number of genes is important for many of these adaptations. Several global expression studies using microarray analysis have been conducted in Arabidopsis thaliana. These studies provide a valuable basis for the identification of new regulatory genes and promoter elements to further the understanding of Pi-dependent gene regulation. With focus on the Arabidopsis transcriptome, we extract common findings that point to new groups of putative regulators, including the NAC, MYB, ethylene response factor/APETALA2, zinc-finger, WRKY and CCAAT-binding families. With a number of new discoveries of regulatory elements, a complex regulatory network is emerging. Some regulatory elements, e.g. the transcription factor PHR1 and the microRNA (miRNA) miR399 and associated factors are well documented, yet not fully understood, whereas other suggested components need further characterisation. Here, we evaluate the contribution of the regulatory elements to the P-responses and present a model comprising factors directly or indirectly involved in transcriptional regulation and the role of miRNAs as regulators and long-distance signals. A striking feature is a series of feedback loops and parallel mechanisms that can modify and attenuate responses. We suggest that these mechanisms are instrumental in providing an accurate response and in keeping P-homeostasis.
Tobacco seedlings were grown in nutrient agar at a range of ammonium nitrate concentrations either without added sucrose, or with 100 mol m -3 sucrose. In the absence of added sucrose, nitrogen-limited plants had increased levels of glucose, fructose and sucrose, decreased chlorophyll, decreased protein, and decreased Rubisco activity, but the level of the transcript for the small subunit of Rubisco (RbcS) did not decrease compared with nitrogen-sufficient plants. When sucrose was added to nitrogen-sufficient seedlings, there was an increase of sucrose, glucose and fructose in the leaves, growth was increased, and the chlorophyll and protein content, Rubisco activity, and the RbcS transcript level did not change. When sucrose was added to nitrogen-limited seedlings, there was a further increase of sucrose, glucose and fructose, growth was not increased, and there was a further decrease of chlorophyll, protein and Rubisco activity, and a marked decrease of the RbcS transcript level. To check that the decrease of the RbcS transcript level was not an indirect effect due to changes of nitrogen metabolites after adding sugars, glucose was added to Chenopodium cells in the presence and absence of glutamine or azaserine. Changes of glutamine that suffice to increase and decrease the level of the transcript for nitrate reductase (Nia) do not affect the RbcS transcript concentration, and glucose addition still led to a decrease of the RbcS transcript level when the internal glutamine concentration was high. Tobacco seedlings were also grown in nutrient agar at a range of phosphate concentrations either without added sucrose, or with 100 mol m -3 sucrose. Phosphate-limited seedlings did not show a decrease of chlorophyll, protein, Rubisco activity, or the level of the RbcS transcript, compared with phosphate-sufficient seedlings. The addition of sucrose to phosphate-limited plants led to a similar increase of sugars to that seen after adding sucrose to nitrogen-limited seedlings, but did not alter chlorophyll, protein, Rubisco activity, or the level of the RbcS transcript. The addition of sucrose to phosphate-limited plants led to a slight increase of the level of the transcript for nitrate reductase (Nia), increased nitrate reductase activity, and a marked increase of the amino acid content. Phosphate limitation led to an increased level of the transcript for the regulatory subunit of ADP glucose pyrophosphorylase (AgpS2), and this response was strengthened when sucrose was added. The regulation of AgpS2 expression by phosphate and sucrose was further investigated by feeding sucrose and phosphate to detached source leaves via the transpiration stream. The level of the AgpS2 transcript decreased after feeding phosphate and increased after feeding sucrose, and the effect of sucrose was antagonised by phosphate. It is concluded that the response to sugar signalling is modulated by nitrogen and phosphate in a gene-specific manner. The significance of these results for understanding the visual phenotype of nitrogen-and phospha...
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