Abstract

Potassium (K) is essential for plant growth and stress responses. MicroRNAs (miRNAs) are involved in adaptation to nutrient deprivation through modulating gene expression. Here, we identified the miRNAs responsive to K deficiency in Triticum aestivum based on high-throughput small RNA sequencing analyses. Eighty-nine miRNAs, including 68 previously reported ones and 21 novel ones, displayed differential expression under K deficiency. In Gene Ontology and Kyoto Encyclopedia and Genome analyses, the putative target genes of the differentially expressed miRNAs were categorized into functional groups associated with ADP-binding activity, secondary metabolic pathways, and biosynthesis and metabolism. Functional characterization of tae-miR408, an miRNA significantly down-regulated under K deficiency, revealed its important role in mediating low-K tolerance. Compared with wild type, transgenic tobacco lines overexpressing tae-miR408 showed significantly improved K uptake, biomass, photosynthesis, and reactive oxygen species scavenging under K deficiency. These results show that distinct miRNAs function in the plant response to K deficiency through regulating target genes involved in energy metabolism and various secondary metabolic pathways. Our findings shed light on the plant response to K deficiency mediated by miRNAs in T. aestivum. Distinct miRNAs, such as tae-miR408, are valuable targets for generating crop varieties with improved K-use efficiency.

Highlights

  • Potassium (K) is a critical inorganic nutrient that is essential for plant growth, development, and yield formation in cereal ­crops[1]

  • MiR408c in soybean is highly induced under Pi-depleted c­ onditions[16]; miR408 in barley mediates the response to low-K via regulation of its target gene encoding blue copper protein (BCP)[9]; and miR408 in cotton post-transcriptionally regulates its target gene encoding Cu/Zn superoxide dismutase 1A under nitrogen deficiency, to improve scavenging of reactive oxygen species (ROS)[17]

  • MiR319 has been recorded to be involved in mediating plant response to Pi starvation ­stress[28], endowing improved plant growth and stress tolerance by regulating chitosan ­metabolism[29] and inhibiting viroid infection into spindle t­uber30. miR398 is down-regulated upon oxidative s­ tress[31], playing an important role in modulating the regulatory networks associated with ROS scavenging, water deficit, salt stress, UV stress, abscisic acid stress, and Cu and Pi ­deprivation[32,33]

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Summary

Introduction

Potassium (K) is a critical inorganic nutrient that is essential for plant growth, development, and yield formation in cereal ­crops[1]. MiR408c in soybean is highly induced under Pi-depleted c­ onditions[16]; miR408 in barley mediates the response to low-K via regulation of its target gene encoding blue copper protein (BCP)[9]; and miR408 in cotton post-transcriptionally regulates its target gene encoding Cu/Zn superoxide dismutase 1A under nitrogen deficiency, to improve scavenging of reactive oxygen species (ROS)[17] These findings suggest that miR408 acts as a crucial regulator and is involved in multiple biological processes. Previous studies to identify members of the miRNA family, characterize their functions in mediating stress responses, and predict their target genes have been extensively performed in model plants, such as Arabidopsis and rice. Our results provide novel insights into the miRNA-mediated adaptation to low-K stress in T. aestivum

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