Control of Jasmonate Biosynthesis and Senescence by miR319 Targets

Abstract

Considerable progress has been made in identifying the targets of plant microRNAs, many of which regulate the stability or translation of mRNAs that encode transcription factors involved in development. In most cases, it is unknown, however, which immediate transcriptional targets mediate downstream effects of the microRNA-regulated transcription factors. We identified a new process controlled by the miR319-regulated clade of TCP (TEOSINTE BRANCHED/CYCLOIDEA/PCF) transcription factor genes. In contrast to other miRNA targets, several of which modulate hormone responses, TCPs control biosynthesis of the hormone jasmonic acid. Furthermore, we demonstrate a previously unrecognized effect of TCPs on leaf senescence, a process in which jasmonic acid has been proposed to be a critical regulator. We propose that miR319-controlled TCP transcription factors coordinate two sequential processes in leaf development: leaf growth, which they negatively regulate, and leaf senescence, which they positively regulate. Short, single-stranded RNA molecules called microRNAs (miRNAs) regulate gene expression by negatively controlling both the stability and translation of target messenger RNAs that they recognize through sequence complementarity. In plants, miRNAs mostly regulate other regulators, the DNA-binding transcription factors. We investigated the downstream events regulated by five TCP (TEOSINTE BRANCHED/CYCLOIDEA/PCF) transcription factors that are controlled by the microRNA miR319 in Arabidopsis thaliana. The miR319-regulated TCPs were previously known to be important for limiting the growth of leaves. By applying a combination of genome-wide, biochemical, and genetic studies, we identified new TCP targets that include enzymes responsible for the synthesis of the hormone jasmonic acid. Our analysis of leaf extracts from plants with increased activity of miR319 confirms that altered expression of the biosynthetic genes leads to changed jasmonic acid levels. These plants show also an altered senescence behavior that becomes more normal again when the plants are treated with jasmonate. We propose that the miR319-regulated TCP factors thus coordinate different aspects of leaf development and physiology: growth, which they negatively regulate, and aging, which they positively regulate.