Abstract
The seed maturation program only occurs during late embryogenesis, and repression of the program is pivotal for seedling development. However, the mechanism through which this repression is achieved in vegetative tissues is poorly understood. Here we report a microRNA (miRNA)–mediated repression mechanism operating in leaves. To understand the repression of the embryonic program in seedlings, we have conducted a genetic screen using a seed maturation gene reporter transgenic line in Arabidopsis (Arabidopsis thaliana) for the isolation of mutants that ectopically express seed maturation genes in leaves. One of the mutants identified from the screen is a weak allele of ARGONAUTE1 (AGO1) that encodes an effector protein for small RNAs. We first show that it is the defect in the accumulation of miRNAs rather than other small RNAs that causes the ectopic seed gene expression in ago1. We then demonstrate that overexpression of miR166 suppresses the derepression of the seed gene reporter in ago1 and that, conversely, the specific loss of miR166 causes ectopic expression of seed maturation genes. Further, we show that ectopic expression of miR166 targets, type III homeodomain-leucine zipper (HD-ZIPIII) genes PHABULOSA (PHB) and PHAVOLUTA (PHV), is sufficient to activate seed maturation genes in vegetative tissues. Lastly, we show that PHB binds the promoter of LEAFY COTYLEDON2 (LEC2), which encodes a master regulator of seed maturation. Therefore, this study establishes a core module composed of a miRNA, its target genes (PHB and PHV), and the direct target of PHB (LEC2) as an underlying mechanism that keeps the seed maturation program off during vegetative development.
Highlights
Seed maturation is a highly coordinated developmental phase in which storage reserves, including seed storage proteins (SSPs), are synthesized and accumulated to high levels
To uncover the molecular mechanisms underlying the repression of seed genes during vegetative development, we performed a reporter-assisted genetic screen, and one mutant identified is a weak allele of ARGONAUTE1 (AGO1) that displays ectopic seed gene expression
We first demonstrate that the decrease in miR166 in ago1 is a major cause of the mutant phenotype
Summary
Seed maturation is a highly coordinated developmental phase in which storage reserves, including seed storage proteins (SSPs), are synthesized and accumulated to high levels. The maturation genes need to be repressed, in order to allow seedling development to occur. These genes are not expressed in vegetative organs of the plant [1]. When misexpressed in vegetative tissues, they induce ectopic expression of the SSP genes and even the formation of somatic embryos [15,17,20,21,22]. It remains poorly understood, how the expression and activity of these master regulators are in turn regulated
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