Abstract
The miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) transcription factors function as an endogenous age cue in regulating plant phase transition and phase-dependent morphogenesis, but the control of SPL output remains poorly understood. In Arabidopsis thaliana the spatial pattern of trichome is a hallmark of phase transition and governed by SPLs. Here, by dissecting the regulatory network controlling trichome formation on stem, we show that the miR171-targeted LOST MERISTEMS 1 (LOM1), LOM2 and LOM3, encoding GRAS family members previously known to maintain meristem cell polarity, are involved in regulating the SPL activity. Reduced LOM abundance by overexpression of miR171 led to decreased trichome density on stems and floral organs, and conversely, constitutive expression of the miR171-resistant LOM (rLOM) genes promoted trichome production, indicating that LOMs enhance trichome initiation at reproductive stage. Genetic analysis demonstrated LOMs shaping trichome distribution is dependent on SPLs, which positively regulate trichome repressor genes TRICHOMELESS 1 (TCL1) and TRIPTYCHON (TRY). Physical interaction between the N-terminus of LOMs and SPLs underpins the repression of SPL activity. Importantly, other growth and developmental events, such as flowering, are also modulated by LOM-SPL interaction, indicating a broad effect of the LOM-SPL interplay. Furthermore, we provide evidence that MIR171 gene expression is regulated by its targeted LOMs, forming a homeostatic feedback loop. Our data uncover an antagonistic interplay between the two timing miRNAs in controlling plant growth, phase transition and morphogenesis through direct interaction of their targets.
Highlights
MicroRNA was first identified as the regulator of the juvenile-to-adult transition in Caenorhabditis elegans [1], and a similar function was later assigned to plant miRNA: miR156 and its target SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) genes define an endogenous aging and flowering pathway [2,3]
By dissecting the regulatory network controlling trichome formation on stem, we show that a group of GRAS family members, LOST MERISTEMS 1 (LOM1), LOM2 and LOM3, targeted by timing miR171, function in modulating the SPL activity through direct protein-protein interaction
MIR171A gene expression is regulated by its own targets (LOMs), forming a feedback loop to program plant life
Summary
MicroRNA (miRNA) was first identified as the regulator of the juvenile-to-adult transition in Caenorhabditis elegans [1], and a similar function was later assigned to plant miRNA: miR156 and its target SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) genes define an endogenous aging and flowering pathway [2,3]. The miR156 overexpression delays phase transition and startup of flowering. In Arabidopsis there are 17 SPL genes, 11 of which contain a miR156 target site. The miR156-targeted SPLs can be divided into four clades based on their protein structures, and the clades composed of SPL3/4/5 and SPL9/15 both promote phase transition [2,3,4]. Acting downstream of miR156-targeted SPLs, miR172 plays roles in developmental timing of Arabidopsis [3]. There are other transcription regulators that affect SPL activities, such as DELLAs, the negative regulator of gibberellin signaling pathway, interact with SPLs to control flowering [5]
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