Abstract

Integrating carbon (C), nitrogen (N), and sulfur (S) metabolism is essential for the growth and development of living organisms. MicroRNAs (miRNAs) play key roles in regulating nutrient metabolism in plants. However, how plant miRNAs mediate crosstalk between different nutrient metabolic pathways is unclear. In this study, deep sequencing of Arabidopsis thaliana small RNAs was used to reveal miRNAs that were differentially expressed in response to C, N, or S deficiency. Comparative analysis revealed that the targets of the differentially expressed miRNAs are involved in different cellular responses and metabolic processes, including transcriptional regulation, auxin signal transduction, nutrient homeostasis, and regulation of development. C, N, and S deficiency specifically induced miR169b/c, miR826 and miR395, respectively. In contrast, miR167, miR172, miR397, miR398, miR399, miR408, miR775, miR827, miR841, miR857, and miR2111 are commonly suppressed by C, N, and S deficiency. In particular, the miRNAs that are induced specifically by a certain nutrient deficiency are often suppressed by other nutrient deficiencies. Further investigation indicated that the modulation of nutrient-responsive miRNA abundance affects the adaptation of plants to nutrient starvation conditions. This study revealed that miRNAs function as important regulatory nodes of different nutrient metabolic pathways.

Highlights

  • To cope with nutrient-deprived environments, plants must sense changes in the external and internal mineral nutrient concentrations and adjust their nutrient metabolisms to meet the demands of plant growth. miRNAs are enriched in the vascular tissues[30,31] where the translocation and distribution of nutrients occurs. miR399 is a long-distance signal for phosphate homeostasis[32]

  • S deficiency, 10-day-old seedlings grown on full nutrient (FN), sucrose-free (–C), nitrogen-free (–N), or sulfate-free (–S) MS medium were used to construct small RNA libraries

  • More than 85% of total sequences were perfectly mapped to the genome, which were further clustered into 11 classes, including exon_antisense, exon_sense, intron_sense, intron_antisense, miRNA, rRNA, repeat, snRNA, snoRNA, tRNA and unannotation (Table 1)

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Summary

Introduction

MiR395 and miR399 mediate the regulation of sulfate and phosphate homeostasis, respectively[21,22]. Copper (Cu) starvation induces miR397, miR398, miR408, and miR857 and mediates the downregulation of copper proteins. MiR827 plays pivotal roles in regulating phosphate homeostasis in plants in a nitrate-dependent fashion[27]. Deep sequencing identified some nutrient-responsive miRNAs, such as miR778, miR828, and miR2111, which were induced during phosphate limitation[28,29]. Nutrient-responsive miRNAs might play crucial roles in modulating nutrient starvation responses and crosstalk among nutrient metabolic pathways. How plant miRNAs mediate the interaction and crosstalk among different nutrient metabolisms remains unknown. This study confirmed that a large number of miRNAs are responsive to nutrient deficiencies and some of them mediate the interaction between different nutrient metabolic pathways

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